Population genetics of P transposable elements and their host species, with emphasis on Drosophila willistoni and Drosophila sturtevanti

Abstract

The evolution of the P element family was studied in members of the Drosophila willistoni and Drosophila saltans species groups (subgenus Sophophora). The transmission of P elements among species, their spread within species and the strength of selective constraints, as well as the level at which they are imposed on these elements, were investigated using DNA sequence data. Particular emphasis was placed on the evolution of the canonical P element subfamily. This subfamily includes the functional P element first isolated from Drosophila melanogaster, which was termed canonical. It includes also other P elements belonging to the saltans and willistoni groups that are closely related to it. Based on the divergence among canonical elements, it was estimated that they last shared a common ancestor 3 million years ago, and that a minimum of eleven horizontal transfer events among species have taken place since then. This indicates that horizontal transfer is more important than anticipated in the transmission of P elements among species. The evolution of P elements within species was studied in detail in Drosophila sturtevanti and Drosophila willistoni. First, the population structure of these species was inferred from nuclear (alcohol dehydrogenase) and mitochondrial (part of subunits 4 and 5 of NADH dehydrogenase, and the transfer RNA gene for histidine) markers. The results suggest that only peripheral populations of D. willistoni show significant genetic differentiation. In D. sturtevanti significant population subdivision was detected among populations in the central part of the distribution, as well as between these and peripheral populations. These results were used as a reference to which P element divergence among populations could be compared. No selective constraints were detected in the evolution of canonical P elements within these two species. However, those constraints are present when elements were compared between species. It is concluded that selection is mostly effective at the time of horizontal transmission between species. Furthermore, P elements are shown to spread faster among populations than do neutral markers. This suggests that the spread of P elements within species can be achieved quickly, and surpass barriers such as moderate levels of population structuring within a species.