Examining the evolutionary arms race between transposons and genome defense provided by the piRNA pathway

Abstract

Transposable elements (TEs) are often referred to as selfish elements that cause harmful mutations by their mobilization in genome. TEs use a “copy and paste” or "cut and paste" mechanism that allows rapid exponential growth within populations, and these TE insertions result in many harmful mutations. Thus, scientists are interested in understanding what prevents TEs from unlimited proliferation. Natural selection has long been considered to be a major factor controlling spread of TEs. Recently, genome defense by the piRNA pathway has proved to be another key mechanism in controlling TEs’ proliferation. A recent study of the molecular evolution of the piRNA pathway indicated that several piRNA genes show a high rate of adaptive evolution rate (Obbard, Gordon et al. 2009). Thus, we predict that there probably is an evolutionary arms race between TEs and the genome defense provided by the piRNA machinery. Like host-parasite dynamics, co-evolution could be driven by adaptions and counter-adaptions in TEs and the piRNA pathway. However, a previous study has shown that the piRNA machinery in Drosophila species with higher TE content show greater levels of purifying selection (Castillo, Mell et al. 2011). Interestingly, they found that codon bias is increased in the piRNA genes of Drosophila species with higher TE abundance. These results may indicate that there is an evolutionary arms race between TEs and host defense provided by the piRNA machinery on expression level instead of protein level. However, it is not clear how general their results are due to 1) only a handful piRNA genes were identified at that time and 2) they only conducted a test using codon bias but gene expression level was not taken into account. Thus, we performed an analysis of both codon bias and gene expression in all known components of the piRNA machinery and tested whether the piRNA machinery evolves a higher expression level in Drosophila species with higher TE content. Our results show piRNA components evolve both higher gene expression and higher codon bias levels in Drosophila species with higher TE load when compared other genes. However, this trend appears to be driven by only a few Drosophila lineages. Greater phylogenetic sampling is needed to determine if this signature is robust to phylogenetic non-independence.