piRNA clusters need a minimum size to control transposable element invasions

Abstract piRNA clusters are thought to repress transposable element activity in mammals and invertebrates. Here we show that a simple population genetics model reveals a constraint on the size of piRNA clusters: the total size of the piRNA clusters of an organism ought to exceed 0.2% of a genome. Larger piRNA clusters accounting for up to 3% of the genome may be necessary when populations are small, transposition rates are high and TE insertions recessive. If piRNA clusters are too small the load of deleterious TE insertions accumulating during a TE invasion may drive populations extinct before an effective piRNA based defence against the TE can be established. Our finding is solely based on three well supported assumptions: i) TEs multiply withing genomes, ii) TEs are mostly deleterious and iii) piRNA clusters act as transposons traps, where a single insertion in a cluster silences all TE copies in trans. Interestingly, piRNA clusters of some species meet our minimum size requirements while clusters of other species don’t. Species with small piRNA clusters, such as humans and mice, may experience severe fitness reductions during invasions of novel TEs, possibly even threatening the persistence of some populations. This work also raises the important question of how piRNA clusters evolve. We propose that the size of piRNA clusters may be at an equilibrium between evolutionary forces that act to expand and contract piRNA clusters.