Regulatory logic and transposable element dynamics in Caenorhabditis genomes

Abstract

Genome sequencing has revealed a tremendous diversity of transposable elements (TEs) in eukaryotes but there is little understanding of the evolutionary processes responsible for these patterns. Theoretical studies predict interactions between elements can regulate TE proliferation but the narrow conditions are at odds with the abundance of TEs in natural populations. We implemented three models of TE regulation in stochastic simulations to analyze how regulatory logic interacted with population genetic factors including reproduction through outcrossing or self-fertility. We focused on autonomous TEs containing the recognition sequences and enzymes necessary for transposition and their non-autonomous relatives, elements that have lost this physical machinery. We found that large outcrossing populations evolving with either Negative Epistatic interactions between autonomous TEs or Asymmetric regulation between autonomous and non-autonomous elements stably maintained TEs. Small or self-fertile populations and those in which TEs moderately impacted fitness or inserted at high rates experienced TE proliferation to the point of population extinction, suggesting high selective pressure for mutational inactivation of TEs. We tested our model predictions in Caenorhabditis genomes by annotating TEs in two focal families, autonomous LINEs and their non-autonomous SINE relatives and the DNA transposon Mutator. We found variation in autonomous - non-autonomous relationships and rapid mutational decay in the sequences allowing TEs to transpose. Together, our results suggest that individual TE families evolve according to disparate regulatory rules relevant in the early, acute stages of TE invasion.