Given that transposons are so abundant in mammalian genomes, it is natural
to assume that through their maintenance the host gains some net benefit. T
his need not be true; sexual reproduction allows a transposon to go to fixa
tion if the reduction in fitness of the host is anything less than two-fold
. Obligate outcrossing sexual reproduction therefore favors the evolution o
f aggressive transposons, which in turn select for the evolution of host me
chanisms that suppress transposon activity. Hosts that have asexual or self
-fertilizing generations will select for transposons that are more benign a
nd self-limiting than those of obligate sexuals, and obligate asexuals and
uniparental organelle genomes will be free of active transposons if these i
mpose any fitness penalty. We are interested in host mechanisms that suppre
ss transposons in sexuals and have found that mammals (all of which are obl
igate sexuals) control their large populations of potentially active retrop
osons by methylating the five position of cytosine residues within promoter
elements. This causes strong transcriptional repression and assembly of th
e affected sequences into the condensed state. Methylation also causes perm
anent 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 o
f the very large transposon burden. There is pressure on transposons to evo
lve 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 c
aused the amount of reverse transcriptase coding sequence in the human geno
me to far exceed the sum total of all cellular coding sequence. While trans
posons could, in principle, contribute functions useful to the host, the fa
ct that asexual species and uniparental organelle genomes lack transposons
is strong evidence that transposons have a net deleterious effect even in g
enomes that might be thought to require an additional source of plasticity.
The abundance of transposons in many genomes cannot be taken as evidence o
f a mutualistic relationship, and the conflict between transposons and geno
mes may have actually retarded rather than accelerated evolution. It is sug
gested that the relationship between sex and transposons is as follows: (i)
Obligate sexuals will tend to harbor aggressive transposons limited largel
y by host suppressive mechanisms, which in mammals involve methylation of t
ransposon 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 unipa
rental manner will have no active transposons if these have a net negative
effect on host fitness.