On the origin of the P-element invasion in Drosophila simulans.

Abstract

The horizontal transfer (HT) of the P-element is one of the best documented cases of the HT of a transposable element. The P-element invaded natural D. melanogaster populations between 1950 and 1980 following its HT from Drosophila willistoni, a species endemic to South and Central America. Subsequently, it spread in D. simulans populations between 2006 and 2014, following a HT from D. melanogaster. The geographic region where the spread into D. simulans occurred is unclear, as both involved species are cosmopolitan. The P-element differs between these two species by a single base substitution at site 2040, where D. melanogaster carries a 'G' and D. simulans carries an 'A'. It has been hypothesized that this base substitution was a necessary adaptation that enabled the spread of the P-element in D. simulans, potentially explaining the 30-50-year lag between the invasions of D. melanogaster and D. simulans. To test this hypothesis, we monitored the invasion dynamics of P-elements with both alleles in experimental populations of D. melanogaster and D. simulans. Our results indicate that the allele at site 2040 has a minimal impact on the invasion dynamics of the P-element and, therefore, was not necessary for the invasion of D. simulans. However, we found that the host species significantly influenced the invasion dynamics, with higher P-element copy numbers accumulating in D. melanogaster than in D. simulans. Finally, based on SNPs segregating in natural D. melanogaster populations, we suggest that the horizontal transfer of the P-element from D. melanogaster to D. simulans likely occurred around Tasmania.