Evolutionary history of LTR-retrotransposons among 20 Drosophila species

Abstract

Background: The presence of transposable elements (TEs) in genomes is known to explain in part the variations of genome sizes among eukaryotes. Even among closely related species, the variation of TE amount may be striking, as for example between the two sibling species, Drosophila melanogaster and D. simulans. However, not much is known concerning the TE content and dynamics among other Drosophila species. The sequencing of several Drosophila genomes, covering the two subgenus Sophophora and Drosophila, revealed a large variation of the repeat content among these species but no much information is known concerning their precise TE content. The identification of some consensus sequences of TEs from the various sequenced Drosophila species allowed to get an idea concerning their variety in term of diversity of superfamilies but the used classification remains very elusive and ambiguous.

Results: We choose to focus on LTR-retrotransposons because they represent the most widely represented class of TEs in the Drosophila genomes. In this work, we describe for the first time the phylogenetic relationship of each LTR-retrotransposon family described in 20 Drosophila species, compute their proportion in their respective genomes and identify several new cases of horizontal transfers.

Conclusion: All these results allow us to have a clearer view on the evolutionary history of LTR retrotransposons among Drosophila that seems to be mainly driven by vertical transmissions although the implications of horizontal transfers, losses and intra-specific diversification are clearly also at play.

Keywords: Drosophila; Horizontal transfer; LTR-retrotransposons; Transposable element dynamics.

Fig. 1

Maximum likelihood phylogenetic tree based on the polyprotein amino acid sequences of Ty1/Copia elements. Only bootstrap values greater than 50% (red dots) or greater than 70% (black dot) are indicated. The tree has been rooted by the BEL element from D. melanogaster. The names of the species are abbreviated as follows: DAn, D. ananassae; DBi, D. biarmipes; DBp, D. bipectina; DEl, D. elegans; DEu, D. eugracilis; DFi, D. ficusphila; DGri, D. grimshawi; DKi, D. kikkawai; DMel, D. melanogaster (in red); DMoj/Dmoj; D. mojavensis; DPer/DP, D. persimilis; Dpse, D. pseudoobscura; DSe, D. sechellia (in green); DSi, D. simulans (in blue); DTa, D. takahashi; DVir, D. virilis; DWil, D. willistoni; Dya/DY, D. yakuba (in pink). Four sequences from other organisms are included. Yellow stars represent cases of confirmed horizontal transfers (see details in Additional file 3: Figure S1a)

Fig. 2

Maximum likelihood phylogenetic tree based on the polyprotein amino acid sequences of BEL/Pao elements. Only bootstrap values greater than 50% (red dots) and greater than 70% (black dot) are indicated. The tree has been rooted by the COPIA element from D. melanogaster. The names of the species are abbreviated as follows: DAn, D. ananassae; DBi, D. biarmipes; DBp, D. bipectina; DEl, D. elegans; DEre, D. erecta (in yellow); DEu/Deu, D. eugracilis; DFi, D. ficusphila; DGri, D. grimshawi; DKi, D. kikkawai; DMel, D. melanogaster (in red); DMir, D. miranda; DMoj/Dmoj/Dmo/DM, D. mojavensis; DPer/Dpe/DP, D. persimilis; DPse/Dpse, D. pseudoobscura; DRh, D. rhopaloa; DSe, D. sechellia (in green); DSi, D. simulans (in blue); DTa, D. takahashi; DVir/DV, D. virilis; DWil, D. willistoni; DYa, D. yakuba (in pink). Four sequences from other insects are included. Yellow stars represent cases of confirmed horizontal transfers (see details in Additional file 3: Figure S1b)

Fig. 3

Maximum likelihood phylogenetic tree based on the polyprotein amino acid sequences of Ty3/Gypsy elements from the group “OSVALDO/ULYSSES”. Only bootstrap values greater than 50% (red dots) and greater than 70% (black dot) are indicated. The tree has been rooted by the Batumi element from D. melanogaster and we also added elements from the two other groups of Ty3/Gypsy (Tirant and BLASTOPIA from D. melanogaster). The names of the species are abbreviated as follows: DAn, D. ananassae; DBi, D. biarmipes; DBp, D. bipectina; Dbuz, D. buzzatti; DEl, D. elegans; DEu/Deu, D. eugracilis; DFi, D. ficusphila; DGri/DG, D. grimshawi; DKi, D. kikkawai; DMel, D. melanogaster (in red); DMoj/Dmoj, D. mojavensis; DPer/DP, D. persimilis; DPse/Dpse, D. pseudoobscura; DRh, D. rhopaloa; DSe, D. sechellia (in green); DSi, D. simulans (in blue); DTa, D. takahashi; DVir/DV, D. virilis; DWil, D. willistoni; DYa/DY, D. yakuba (in pink). Yellow stars represent cases of confirmed horizontal transfers (see details in Additional file 3: Figure S1c)

Fig. 4

Maximum likelihood phylogenetic tree based on the polyprotein amino acid sequences of Ty3/Gypsy elements from the group “MICROPIA/SACCO”. Only bootstrap values greater than 50% (red dots) and greater than 70% (black dot) are indicated. The tree has been rooted by the Batumi element from D. melanogaster and we also added elements from the two other groups of Ty3/Gypsy (Tirant from D. melanogaster and Osvaldo from D. buzzati). The names of the species are abbreviated as follows: DAn, D. ananassae; DBi, D. biarmipes; DBp, D. bipectina; Dbuz, D. buzzatti; DEl, D. elegans; DEre, D. erecta; DEu/Deu, D. eugracilis; DFi, D. ficusphila; DMel, D. melanogaster (in red); Dmoj, D. mojavensis; DPer/DP, D. persimilis; Dpse, D. pseudoobscura; DRh, D. rhopaloa; DSe, D. sechellia (in green); DSi, D. simulans (in blue); DTa, D. takahashi; DVir/DV, D. virilis; DWil, D. willistoni; DYa/Dya, D. yakuba (in pink). Two sequences from other insects are included. Yellow stars represent cases of confirmed horizontal transfers (see details in Additional file 3: Figure S1d)

Fig. 5

Maximum likelihood phylogenetic tree based on the polyprotein amino acid sequences of Ty3/Gypsy elements from the group “errantiviridae/412”. Only bootstrap values greater than 50% (red dots) and greater than 70% (black dot) are indicated. The tree has been rooted by the Batumi element from D. melanogaster and we also added elements from the two other groups of Ty3/Gypsy (Blastopia from D. melanogaster and Osvaldo from D. buzzati). The names of the species are abbreviated as follows: DAn, D. ananassae; DBi, D. biarmipes; DBp, D. bipectina; Dbuz, D. buzzatti; DEl, D. elegans; DEre, D. erecta; DEu/Deu, D. eugracilis; DFi, D. ficusphila; DGri/DG, D. grimshawi; DKi, D. kikkawai; Dmel/DM, D. melanogaster (in red); DMoj/Dmoj, D. mojavensis; Dpse, D. pseudoobscura; DRh, D. rhopaloa; Dse, D. sechellia (in green); Dsi, D. simulans (in blue); DTa, D. takahashi; DVir, D. virilis; DWil, D. willistoni; DY/Dya, D. yakuba (in pink). Two sequences from other insects are included. Yellow stars represent cases of confirmed horizontal transfers (see details in Additional file 3: Figure S1d and e)

Fig. 6

Proportion (in %) in the genomes of the 20 Drosophila species of each superfamily of LTR retrotransposons. The intensity of the blue colors is proportional to the TE proportion. The species are presented according to the phylogenetic tree topology as proposed by Seetharam & Stuart 2013, and we have indicated the genome sizes of each sequenced genome