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. 2016 Apr;33(4):1094-109.
doi: 10.1093/molbev/msv341. Epub 2015 Dec 18.

VHICA, a New Method to Discriminate between Vertical and Horizontal Transposon Transfer: Application to the Mariner Family within Drosophila

Gabriel Luz Wallau  1 , Pierre Capy  2 , Elgion Loreto  3 , Arnaud Le Rouzic  2 , Aurélie Hua-Van  2
Affiliations

VHICA, a New Method to Discriminate between Vertical and Horizontal Transposon Transfer: Application to the Mariner Family within Drosophila

Gabriel Luz Wallau et al. Mol Biol Evol. 2016 Apr.

Abstract

Transposable elements (TEs) are genomic repeated sequences that display complex evolutionary patterns. They are usually inherited vertically, but can occasionally be transmitted between sexually independent species, through so-called horizontal transposon transfers (HTTs). Recurrent HTTs are supposed to be essential in life cycle of TEs, which are otherwise destined for eventual decay. HTTs also impact the host genome evolution. However, the extent of HTTs in eukaryotes is largely unknown, due to the lack of efficient, statistically supported methods that can be applied to multiple species sequence data sets. Here, we developed a new automated method available as a R package "vhica" that discriminates whether a given TE family was vertically or horizontally transferred, and potentially infers donor and receptor species. The method is well suited for TE sequences extracted from complete genomes, and applicable to multiple TEs and species at the same time. We first validated our method using Drosophila TE families with well-known evolutionary histories, displaying both HTTs and vertical transmission. We then tested 26 different lineages of mariner elements recently characterized in 20 Drosophila genomes, and found HTTs in 24 of them. Furthermore, several independent HTT events could often be detected within the same mariner lineage. The VHICA (Vertical and Horizontal Inheritance Consistence Analysis) method thus appears as a valuable tool to analyze the evolutionary history of TEs across a large range of species.

Keywords: Drosophila; codon usage; horizontal transfer; mariner element; synonymous substitutions; transposable elements; vertical transmission.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.
Comparison of a dS-only-based method (left bars chart) and the method proposed in this work (ENC–dS correlation graph in the right side of the figure). White circles represent the 50 host genes used as our control for vertically transmitted genetic information, red circles are the TE ENC–dS plotted against the vertically inherited host genes, the dotted black line represents the predicted distribution of the ENC–dS correlation between host genes derived from the observed data, and the dotted red line represents the variance of the observed measurements. If the TE ENC–dS red circle is plotted inside of the variance of the host data, then it is not significantly different from the host genes and it is considered vertically transmitted. On the contrary, if it is plotted far from the dotted red line it is significantly different from the host genes, hence it will be considered horizontally transferred between the two species. dS, number of synonymous substitutions per synonymous sites; ENC, Effective Number of Codons.
F<sc>ig</sc>. 2.
Fig. 2.
Interpretation of theoretical patterns for the graphical matrix view with four fictive species (A–D). The green tree represents the host (species) tree and the overlapping black tree corresponds to the TE tree. TE loss is represented by an “X” over the species tree, and HTT event is indicated by a red arrow. The expected divergences between species are plotted on a scale below the tree, and appear in green for host genes (HG), and in black for TEs. The matrix of squares on the right represents all pairwise comparisons. Each square is colored according to the color bar of the P value calculated for the null hypothesis of vertical transmission. For simplicity, we assumed here that the statistical power was identical in all pairwise comparisons, so that the P value reflects directly the divergence difference between genes and TE. (A) TEs are vertically transmitted. (B) Recent HTT from species B to A associated with the loss of ancestral copies in species A. (C) Old horizontal transfer between the ancestor of species D and the ancestor of B and C. (D) Recent HTT from species A to B.
F<sc>ig</sc>. 3.
Fig. 3.
Phylogenetic reconstruction for the 20 Drosophila sequenced genomes. (A) Phylogeny built by a Bayesian analysis using the GTR+I+G nucleotide substitution model. (B) and (C) are the phylogenies from the literature. (D) The consensus tree used for HTT analysis.
F<sc>ig</sc>. 4.
Fig. 4.
(A) Species tree phylogeny presenting the distribution of the P elements in Drosophila. Black branches indicate absence of the element. (B) P elements ML-tree following the species-specific color from part (A), and showing the different group/type of P elements (GTR+I+G). Bootstraps (1,000 replicates) are indicated below branches, and the subfamilies numbering above the branches (a:i). Stars denote representative copies used in the study. (C) Simplified phylogeny obtained with these elements. Names include the species names and the subfamily. (D) Consistency graphical representation for the P element. Each square represents one species comparison. When several elements are analyzed for one species (sublineages), the square is divided into rectangles, each one represents one sublineage. Sublineages are indicated on the sides. The horizontal transfer between Drosophila melanogaster and D. willistoni concerns elements of the subfamily a only, and is then visible as a small red rectangle. Other rectangles from this square correspond to comparisons between the D. melanogaster element (sublineage a) and the other elements (sublineages b,d,i) from D. willistoni. (E) ENC–dS graph between D. melanogaster and D. willistoni showing the P HTT transfer. Open circles represent the ENC–dS measures of the 50 single copy ortholog genes. The dotted black line represents the linear regression of ENC–dS from genes, and the dotted red line corresponds to the cutoff P value of 0.05. TE comparisons are figured as red triangles: P.a is the comparison of sequences from the a sublineage. Other comparisons are between the D. melanogaster P element from sublineage a with D. willistoni elements from sublineages b, d, or i (P.a.b, P.a.d, P.a.i).
F<sc>ig</sc>. 5.
Fig. 5.
vhica analysis for elements already described in the literature for horizontal transfer and vertical transmission.
F<sc>ig</sc>. 6.
Fig. 6.
Detailed analysis for two mariner lineages: Dromar8 (A–E) and Dromar6 (F–H). (A) and (F) Distribution of Dromar8 and Dromar6 in Drosophila, with indications of copy number and lineages with potentially active copies (data from Wallau et al. 2014). (B) and (G) TE phylogenies of Dromar8 and Dromar6 with stars denoting the representative copies (Evolutionary models were HKY+I+G and TPM3uf+G, respectively). (D and H) HTT matrices generated by vhica. (E) ENC–dS plot obtained from the comparison between the two species in which Dromar8 has amplified. (C) Amplification dynamics analysis of Dromar8 in the two species with large copy numbers (see Le Rouzic et al. 2013 for a full description of the method).
F<sc>ig</sc>. 7.
Fig. 7.
ENC–dS plot obtained for closely related-species (Drosophila ananassae × D. bipectinata, and D. simulans × D. erecta) and more distantly related species (D. ficusphila × D. bipectinata, D. melanogaster × D. mojavensis). White circles represent host genes and red triangles are TEs. The dotted black line is the linear regression, and the dotted red lines the cutoff P value of 0.05.
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