Transpositional shuffling and quality control in male germ cells to enhance evolution of complex organisms

Complex organisms, particularly mammals, have long generation times and produce small numbers of progeny that undergo increasingly entangled developmental programs. This reduces the ability of such organisms to explore evolutionary space, and, consequently, strategies that mitigate this problem likely have a strategic advantage. Here, we suggest that animals exploit the controlled shuffling of transposons to enhance genomic variability in conjunction with a molecular screening mechanism to exclude deleterious events. Accordingly, the removal of repressive DNA-methylation marks during male germ cell development is an evolved function that exploits the mutagenic potential of transposable elements. A wave of transcription during the meiotic phase of spermatogenesis produces the most complex transcriptome of all mammalian cells, including genic and noncoding sense-antisense RNA pairs that enable a genome-wide quality-control mechanism. Cells that fail the genomic quality test are excluded from further development, eventually resulting in a positively selected mature sperm population. We suggest that these processes, enhanced variability and stringent molecular quality control, compensate for the apparent reduced potential of complex animals to adapt and evolve.