Geography-Dependent Horizontal Gene Transfer from Vertebrate Predators to Their Prey

Abstract

Horizontal transfer (HT) of genes between multicellular animals, once thought to be extremely rare, is being more commonly detected, but its global geographic trend and transfer mechanism have not been investigated. We discovered a unique HT pattern of Bovine-B (BovB) LINE retrotransposons in vertebrates, with a bizarre transfer direction from predators (snakes) to their prey (frogs). At least 54 instances of BovB HT were detected, which we estimate to have occurred across time between 85 and 1.3 Ma. Using comprehensive transcontinental sampling, our study demonstrates that BovB HT is highly prevalent in one geographical region, Madagascar, suggesting important regional differences in the occurrence of HTs. We discovered parasite vectors that may plausibly transmit BovB and found that the proportion of BovB-positive parasites is also high in Madagascar where BovB thus might be physically transported by parasites to diverse vertebrates, potentially including humans. Remarkably, in two frog lineages, BovB HT occurred after migration from a non-HT area (Africa) to the HT hotspot (Madagascar). These results provide a novel perspective on how the prevalence of parasites influences the occurrence of HT in a region, similar to pathogens and their vectors in some endemic diseases.

Keywords: biogeography; horizontal transfer; parasite-dependent transmission; predator and prey; retrotransposons.

Fig. 1.

Phylogeny, ages, and geographic distribution of HTs of squamate-type BovB. (a) The nine biogeographic areas defined in this study. Numbers at each region on the map indicate the numbers of HTs among reptiles and amphibians occurring within the past 50 Ma (33 of total 54 HTs). (b) The animal taxa surveyed (reptile, blue; frog, green; mammal, orange; and parasite, red). (c) The time tree of BovBs from 222 OTUs with HT occurrence geographic region estimated by BioGeoBEARS. Each tip of the tree is color-coded according to distribution within nine world regions (left, the color code is the same with a) and taxa (right = b). Pie charts on nodes represent the relative probabilities of occurrence areas for the 54 possible HTs. Reconstructions resulting in more than two possible regions are shown in dark gray. The compartments marked with Roman numerals correspond to those in d. (d) The topologies show remarkable HTs. Numbers at nodes indicate divergence time (Ma). The blindsnakes and Malagasy boas are labeled by capital letters in parentheses (T—Typhlopidae and B—Boidae, respectively). The gray-colored animal symbols represent the hosts of BovB-positive parasites. The arrows with small letters correspond to those in figure 2.

Fig. 2.

Transmission pathways of snake BovBs via parasites. The representatives of HTs of snake BovBs via parasites are shown. The thick and thin arrows show the direction of HT and the similarities of BovB sequences between taxa, respectively.