Population genomics supports baculoviruses as vectors of horizontal transfer of insect transposons

Abstract

Horizontal transfer (HT) of DNA is an important factor shaping eukaryote evolution. Although several hundreds of eukaryote-to-eukaryote HTs of transposable elements (TEs) have been reported, the vectors underlying these transfers remain elusive. Here, we show that multiple copies of two TEs from the cabbage looper (Trichoplusia ni) transposed in vivo into genomes of the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) during caterpillar infection. We further demonstrate that both TEs underwent recent HT between several sympatric moth species (T. ni, Manduca sexta, Helicoverpa spp.) showing different degrees of susceptibility to AcMNPV. Based on two independent population genomics data sets (reaching a total coverage >330,000X), we report a frequency of one moth TE in ~8,500 AcMNPV genomes. Together, our results provide strong support for the role of viruses as vectors of TE HT between animals, and they call for a systematic evaluation of the frequency and impact of virus-mediated HT on the evolution of host genomes.

Figure 1. Map of transposable element copies integrated in the genome of the AcMNPV baculovirus.

Integrations took place both in the positive (+) and the negative (−) strand of the viral genome after passage of AcMNPV in T. ni larvae. (a) MAR1, IFP2 and HaSE3 insertions recovered in AcMNPV genomes sequenced at 187,536X coverage (Data set 1). (b) MAR1 and IFP2 insertions recovered in AcMNPV genomes sequenced at 145,386X total coverage (Data set 3).

Figure 2. Phylogenies of the two transposons found integrated in the AcMNPV genome.

(a) Tree of MAR1 copies. Scale bar for the branch length is 0.01 substitution per site. (b) Tree of IFP2 copies. Scale bar for the branch length is 0.1 substitution per site. Bootstrap values >70% are shown on branches. The numbers of copies used for phylogenetic analysis are shown in brackets for each species. For each tree, the AcMNPV transposable element corresponds to the consensus sequence of all copies found integrated in the viral genome. The AcMNPV pictures were taken using scanning electron miscroscopy. White scale bar, 1 μm.