TE invasion fuels molecular adaptation in laboratory populations of Drosophila melanogaster

Transposable elements are mobile genetic parasites that frequently invade new host genomes through horizontal transfer. Invading TEs often exhibit a burst of transposition, followed by reduced transposition rates as repression evolves in the host. We recreated the horizontal transfer of P-element DNA transposons into a D. melanogaster host and followed the expansion of TE copies and evolution of host repression in replicate laboratory populations reared at different temperatures. We observed that while populations maintained at high temperatures rapidly go extinct after TE invasion, those maintained at lower temperatures persist, allowing for TE spread and the evolution of host repression. We also surprisingly discovered that invaded populations experienced recurrent insertion of P-elements into a specific long non-coding RNA, lncRNA:CR43651, and that these insertion alleles are segregating at unusually high frequency in experimental populations, indicative of positive selection. We propose that, in addition to driving the evolution of repression, transpositional bursts of invading TEs can drive molecular adaptation.Microsoft Excel or a text editor.Funding provided by: National Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000001Award Number: 1457800Funding provided by: National Institutes of HealthCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000002Award Number: GM138112These data were collected from Drosophila melanogaster populations maintained in the laboratory for 3 years. P-elements were introduced into the populations and the populations were maintained at a census population size of 1,000 individuals. Populations were maintained at 22°C and 27°C. Every five generations, experimental males and females were phenotyped for induction and repression of hybrid dysgenesis through test crosses to the reference strains Canton S (M) and Harwich (P). Ovarian small RNAs were Illumina sequenced at generations 16, 21 26, 31, 36 and 51 for two replicate populations at 22°C. For all populations at 22°C, ovarian small RNAs were sequenced at the final generation of the experiment (Generation 51). Similarly, for all populations at 22°C, 20 females were selected for pooled Illumina genome resequencing. Populations maintained at 27°C went extinct at various times, individuals two of these populations were also resequenced at their extinction generation. Genome resequencing data was used to identify P-element insertion locations and estimate allele frequencies using PIDFE. Ovarian small RNAs were aligned to the reference genome as well as TEs in order to 1) estimate miRNA abundance for normalization, 2) estimate abundance of different TE families in piRNAs, 3) calculate ping-pong values and 4) annotated piRNA clusters and 5) estimate piRNA production from piRNA clusters