Multiple invasions of Gypsy and Micropia retroelements in genus Zaprionus and melanogaster subgroup of the genus Drosophila

Abstract

Background: The Zaprionus genus shares evolutionary features with the melanogaster subgroup, such as space and time of origin. Although little information about the transposable element content in the Zaprionus genus had been accumulated, some of their elements appear to be more closely related with those of the melanogaster subgroup, indicating that these two groups of species were involved in horizontal transfer events during their evolution. Among these elements, the Gypsy and the Micropia retroelements were chosen for screening in seven species of the two Zaprionus subgenera, Anaprionus and Zaprionus.

Results: Screening allowed the identification of diverse Gypsy and Micropia retroelements only in species of the Zaprionus subgenus, showing that they are transcriptionally active in the sampled species. The sequences of each retroelement were closely related to those of the melanogaster species subgroup, and the most parsimonious hypothesis would be that 15 horizontal transfer events shaped their evolution. The Gypsy retroelement of the melanogaster subgroup probably invaded the Zaprionus genomes about 11 MYA. In contrast, the Micropia retroelement may have been introduced into the Zaprionus subgenus and the melanogaster subgroup from an unknown donor more recently (~3 MYA).

Conclusion: Gypsy and Micropia of Zaprionus and melanogaster species share similar evolutionary patterns. The sharing of evolutionary, ecological and ethological features probably allowed these species to pass through a permissive period of transposable element invasion, explaining the proposed waves of horizontal transfers.

Figure 1

Phylogenetic tree of the Drosophilidae family. Phylogenetic relationships between the main Drosophilidae species groups, evidencing the taxonomic positioning of the Zaprionus genus inside the Drosophila subgenus and the divergence time between Drosophila and Sophophora subgenus [redrawn from reference [7]].

Figure 2

Phylogenetic relationships between Gypsy retroelements. Phylogeny of Gypsy sequences of genus Zaprionus (green squares), the melanogaster subgroup (red circles), D. willistoni (blue triangles) and S. latifasciaeformis (pink circles). Numbers in squares indicate the clade number mentioned in the text. The tree was reconstructed using the maximum-likelihood method (HKY85 distance), as implemented in the PhyML program. The branch support was calculated using bootstrap test (1000 replications). Numbers next to species names indicate the clone or genomic sequence identification.

Figure 3

Comparative analysis of dS values of Gypsy and Gpdh. Comparative analyses of the dS values between Gypsy and Gpdh sequences of Zaprionus and melanogaster species within the S1 subfamily, S2V1 and S2V2. tub: Z. tuberculatus, cam: Z. camerounensis, dav: Z. davidi, gab: Z. gabonicus, afr: Z. africanus, ind: Z. indianus, mel: D. melanogaster, sim: D. simulans, sec: D. sechellia, yak: D. yakuba, ere: D. erecta.

Figure 4

Phylogenetic relationships between Micropia retroelements. Phylogeny of Micropia sequences of genus Zaprionus (green squares) and the melanogaster (red circles) and repleta (blue triangles) groups. The trees were reconstructed using the maximum-likelihood method (HKY85 distance), as implemented in the PhyML program. Numbers in squares indicate the clade number mentioned in the text. The branch support was calculated using bootstrap test (1000 replications). Numbers next to species names indicate the clone or genomic sequence identification.

Figure 5

Comparative analysis of dS values of Micropia and Gpdh. Comparative analyses of the dS values between Micropia and Gpdh of Zaprionus and melanogaster species. Comparison with only black column indicates that the synonymous sites of Micropia are invariable. tub: Z. tuberculatus, cam: Z. camerounensis, dav: Z. davidi, gab: Z. gabonicus, afr: Z. africanus, ind: Z. indianus, mel: D. melanogaster, sim: D. simulans, sec: D. sechellia, yak: D. yakuba.

Figure 6

Network reconstructions. Median-joining network analyses for the Zaprionus and the melanogaster species. The size of each circle denotes the number of sequences grouped together. (a) Network for the Gypsy retroelement. Each group obtained in the phylogenetic tree is differently colored. (b) Detail of the Gypsy Subfamily 2. (c) Network for the Micropia retroelement. The sequences are colored according the clustering in the phylogenetic tree. The black arrows show the HT events evidenced by network trees.