Patterns and processes of horizontal DNA transfer: an in-depth exploration of the host-parasitoid route – Horizon

It is now recognised that DNA can move across species barriers, not only in bacteria and archaea, where this has been long-recognised, but also among eukaryotes, including metazoans. In the latter however, Horizontal Transfers (HTs) are only documented from a few case studies, providing us with a highly-fragmented picture of which genetic elements can actually move, and by what processes. Evidence for HT between insect parasitoids and the hosts in which they develop indicates that this tight ecological connectivity can allow the transmission of DNA. Other data sets suggest that Transposable Elements (TEs) tend to be exchanged most frequently between closely related lineages, possibly because of the resemblance between the donor and recipient organisms. Building on these observations, we hypothesize here that ecological connectivity and phylogenetic relatedness represent the major determinants of HT. To test this hypothesis, we will combine full genome sequencing with the results of 40 years of field work in a Costa Rican National Park that have exhaustively documented the network of interactions between Lepidoptera caterpillars and their parasitoids. We take advantage of the DNA-barcoding campaign that has complemented the ecological dataset since 2004, and produced molecular markers and DNA extracts from over 200,000 specimens, distributed across 5000+ species of Lepidoptera and their 2000+ species of parasitoids, both Diptera and Hymenoptera. The available molecular data provides a useful phylogenetic framework which will be used in combination with the ecological network to select 250 species, each represented by two specimens, from which we will produce full genomes. The available DNA extracts are readily usable for full genome sequencing, as demonstrated by a preliminary sequencing experiment that we performed since the submission of our pre-proposal.
In the first year and first Task of the project, we will sequence and assemble the genomes. In the second task, we will document patterns of HT, that is, produce an exhaustive catalogue of transfer events using a combination of two approaches: (1) we will compute the genetic distance at all homologous regions between hosts and parasitoid genomes, to detect very similar sequences, that are indicative of recent host-parasitoid HTs; (2) a more complete picture will be obtained using cophylogenetic approaches (that is, comparisons between species trees and gene-specific trees) that will reveal ancient transfers, as well as transfers between closely related species (e.g. between two hosts or two parasitoids). These analyses will be applied to the various kinds of genetic entities present in our data set: nuclear genomes (distinguishing transposable elements from non-mobile nuclear DNA), intracellular bacteria and viruses. Following this descriptive step of the project, we will be in position to investigate the processes underlying HTs, in the third Task of the project. Specifically, we will test the hypothesis that ecological connectivity and phylogenetic distance are the two major factors affecting the passage of DNA across species. Having assessed the amount of HTs that have occurred between hosts and parasitoids, we will test the correlation between the ecological network and HT patterns. We will also investigate the possibility of HTs between two parasitoids or between two hosts through a shared prey or predator. Using such within-group transfers, we will analyse the relationship between the phylogenetic distance and the rate of HT between lineages. While challenging both in its scale and in the complexity of the questions being addressed, the Horizon project involves a team of highly complementary researchers, datasets and methods, from field ecology to phylogenomics, that will provide major breakthrough in our understanding of horizontal DNA transfer in metazoans, and the possibly vast evolutionary implications of this fascinating phenomenon.