Rapid emergence of non-autonomous elements may stop P-element invasions in the absence of a piRNA-based host defence
Matthew Beaumont, Divya Selvaraju, Riccardo Pianezza, Robert Kofler
Abstract
Transposable element (TE) invasions pose risks to both the TE and the host. All copies of a TE may be lost via genetic drift, or host populations may suffer fitness declines, potentially leading to extinction. By monitoring invasions of the P-element in experimental D. melanogaster populations for over 100 generations, we uncovered a novel risk for invading TEs. In two replicate populations, the P-element rapidly multiplied until a piRNA-based host defence emerged, leading to the plateauing of TE copy numbers.
Introduction
Eukaryotic organisms have long faced the threat of transposable element (TE) invasions. These stretches of DNA integrate into host genomes and selfishly replicate, irrespective of fitness effects [16,57]. TEs have proven extraordinarily effective in self-transmission, having been able to invade almost all observed eukaryotic genomes [6,87]. They show varying success rates in colonising different species, where the total TE content in host genomes ranges from just 3% in yeast, to 78% in Antarctic krill [6,75].
Materials and method
Experimental populations
We introduced the P-element into DM68, a D. melanogaster strain collected 1954 in Israel, via micro-injection of the plasmid ppi25.1 (kindly provided by Dr. Erin Kelleher). Injections were performed by Rainbow Transgenic Flies Inc (https://www.rainbowgene.com/; Camarillo, CA, USA). We obtained 7 lines containing the P-element by crossing transformed adults (2 males and 3 females). Transformed lines were maintained at 20° C for 3 generations before setting up the experimental populations.
Results
P-element invasions in experimental D. melanogaster populations
To study the dynamics of TE invasions, we introduced the P-element, via micro-injection, into a D. melanogaster strain (DM68) without any P-element insertions (S1 Fig). We then established three replicate populations (R1, R2, R3), by mixing transformed flies with naïve DM68 flies. Populations were maintained at a size of N = 250 and a temperature of 25° C, with non-overlapping generations.
Discussion
We introduced the P-element into three replicate populations of D. melanogaster and monitored the following invasion at the level of the genome and transcriptome for over 100 generations. We observed that copy numbers of the P-element stabilised at around 20-25 copies in two replicates (R1, R3), but at only ∼7 copies, in R2. Interestingly, copy numbers stabilised in R2 despite the absence of a piRNA-based host defence (until at least generation 45, from small RNA data). GD assays indicate that a piRNA-based host defence was still absent in R2 at generation 98 (females crossed with Harwich males induced GD; Fig 5D).
Acknowledgments
We thank Erin Kelleher for providing ppi25.1, Almorò Scarpa and all other members of the Institute of Population Genetics for their feedback and support.
Citation: Beaumont M, Selvaraju D, Pianezza R, Kofler R (2025) Rapid emergence of non-autonomous elements may stop P-element invasions in the absence of a piRNA-based host defence. PLoS Genet 21(8): e1011649.
https://doi.org/10.1371/journal.pgen.1011649
Editor: Cédric Feschotte, Cornell University, UNITED STATES OF AMERICA
Received: March 7, 2025; Accepted: July 24, 2025; Published: August 20, 2025
Copyright: © 2025 Beaumont et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Sequencing data generated in this work are available from NCBI (BioProject ID: PRJNA1198884). All analysis performed here is available at: https://github.com/divygenome/Dmel_Pelement_Invasion.
Funding: This research was funded in whole by the Austrian Science Fund (FWF), grants P35093 and P34965 to Dr Robert Kofler. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
