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

Abstract

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.

Type Journal
ISBN 1749-6632 (Electronic) 0077-8923 (Linking)
Authors Werner, A. ; Piatek, M. J. ; Mattick, J. S.;
Responsible Garvan Author Professor John Mattick
Publisher Name Annals of the New York Academy of Sciences
Published Date 2015-01-01
Published Volume 1341
Published Pages 156-63
Status Published in-print
URL link to publisher's version http://www.ncbi.nlm.nih.gov/pubmed/25557795
OpenAccess link to author's accepted manuscript version https://publications.gimr.garvan.org.au/open-access/13382