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. 2004 Nov;168(3):1323-35.
doi: 10.1534/genetics.103.025775.

Evolution of P elements in natural populations of Drosophila willistoni and D. sturtevanti

Joana C Silva  1 , Margaret G Kidwell
Affiliations

Evolution of P elements in natural populations of Drosophila willistoni and D. sturtevanti

Joana C Silva et al. Genetics. 2004 Nov.

Abstract

To determine how population structure of the host species affects the spread of transposable elements and to assess the strength of selection acting on different structural regions, we sequenced P elements from strains of Drosophila willistoni and Drosophila sturtevanti sampled from across the distributions of these species. Elements from D. sturtevanti exhibited considerable sequence variation, and similarity among them was correlated to geographic distance between collection sites. By contrast, all D. willistoni elements sampled were essentially identical (pi < 0.2%) and exhibited patterns typical of a recent population expansion. While the canonical P elements sampled from D. sturtevanti appear to be long-time residents in that species, a rapid expansion of a very young canonical P-element lineage is suggested in D. willistoni, overcoming barriers such as large geographical distances and moderate levels of population subdivision. Between-species comparisons reveal selective constraints on P-element evolution, as indicated by significantly different substitution rates in noncoding, silent, and replacement sites. Most remarkably, in addition to replacement sites, selection pressure appears to be strong in the first and third introns and in the 3' and 5' flanking regions.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
Schematic of the structure of the canonical P. (A) The canonical D. melanogaster P element. The element is flanked by 31-bp inverted terminal repeats (represented by arrows). These are adjacent to 5′ and 3′ terminal regions (represented by single lines). The element has four ORFs, numbered 0–3, which together encode a transposase enzyme. ORFs are represented by open rectangles, and introns by single lines. The first and last positions of each noncoding region are numbered above. The inverted terminal repeats were excluded from all analyses, as they were the primer-binding regions. (B) Structure of the P elements sequenced from stains of D. willistoni and D. sturtevanti. Open boxes represent open reading frames, and horizontal lines represent introns and flanking regions. The location of insertions is marked by a T-shaped sign, and their relative length is indicated by the size of the top of the T. An interruption in the structure of an element represents a large deletion. All the elements sequenced from D. willistoni are complete, except for small indels.
F<sc>igure</sc> 2.—
Figure 2.—
Collection sites of D. willistoni and D. sturtevanti strains. Numbers correspond to the first column of Table 1, where location, date, and collector are specified for each strain.
F<sc>igure</sc> 3.—
Figure 3.—
Phylogenetic relationships of P elements sampled from D. willistoni and D. sturtevanti, reconstructed using maximum parsimony. Elements collected for this study are in boldface type; they are prefixed with “Dwill” or “Dst” for D. willistoni and D. sturtevanti, respectively. All 35 D. willistoni P elements sampled form a monophyletic clade (only two representatives of these are shown in the shaded polygon comprising Dwill sequences); likewise, six D. sturtevanti P elements from Mexico and Central America are monophyletic (two representatives are shown in the shaded polygon comprising Dst sequences). The S. pallida P element and the noncanonical elements from Drosophila lusaltans, Drosophila pavlovskiana, and D. sturtevanti (Dsturtevanti42) were used as outgroups. Encircled letters mark individual clades of D. sturtevanti sequences and are used for reference in the text and tables. One of 2210 most parsimonious trees is shown, with branch lengths proportional to the number of nucleotide changes and bootstrap support shown on the tree. All elements analyzed in this study are part of the canonical clade, with the exception of Matlapa2 from D. sturtevanti.
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References

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