VHICA, a New Method to Discriminate between Vertical and Horizontal Transposon Transfer: Application to theMarinerFamily withinDrosophila

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.

Massive horizontal transfer of transposable elements in insects

“…This unprecedented figure is more than four times higher than the total number of HTT events reported so far in metazoans, plants, and fungi combined (10). Such a high number is still not unexpected, given that studies focusing on one or a few TEs often found one or more HTT events between multiple, distantly related taxa (11,(14)(15)(16)22).…”

“…We identified clades of related insect species for which this situation may happen, by relying on the common assumption that inherited TEs evolve neutrally and similarly to synonymous sites of protein coding genes (20). This assumption implies that TEs showing higher interspecific homology than the synonymous sites of orthologous genes should share a more recent ancestor than the host species, and hence be the result of HT (16,21). Conversely,…”

“…HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,[14][15][16]. However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfers in eukaryotes (13).…”

“…A growing number of studies have identified such HTT (11,(14)(15)(16). However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfers in eukaryotes (13). In this study, we overcame these limitations by performing a large-scale, comprehensive analysis of HTT in insects.…”

Characterization of Herves‐like transposable elements (hATs) in Drosophila species and their evolutionary scenario

“…For species for which genomes are available, HTT was estimated using the vhica R package (Wallau et al ., ). As can be seen in Fig.…”