Abstract
Transposable elements (TEs) are highly abundant in the genome and capable of mobility, two properties that make them particularly prone to transfer horizontally between organisms. Although the impact of horizontal transfer (HT) of TEs is well recognized in prokaryotes, the frequency of this phenomenon and its contribution to genome evolution in eukaryotes remain poorly appreciated. Here, we provide evidence that a DNA transposon called SPIN has colonized the genome of 17 species of reptiles representing nearly every major lineage of squamates, including 14 families of lizards, snakes, and amphisbaenians. Slot blot analyses indicate that SPIN has amplified to high copy numbers in most of these species, ranging from 2,000-28,000 copies per haploid genome. In contrast, we could not detect the presence of SPIN in any of the turtles (seven species from seven families) and crocodiles (four species) examined. Genetic distances between SPIN sequences from species belonging to different squamate families are consistently very low (average = 0.1), considering the deep evolutionary divergence of the families investigated (most are >100 My diverged). Furthermore, these distances fall below interfamilial distances calculated for two genes known to have evolved under strong functional constraint in vertebrates (RAG1, average = 0.24 and C-mos, average = 0.27). These data, combined with phylogenetic analyses, indicate that the widespread distribution of SPIN among squamates is the result of at least 13 independent events of HTs. Molecular dating and paleobiogeographical data suggest that these transfers took place during the last 50 My on at least three different continents (North America, South America and, Africa). Together, these results triple the number of known SPIN transfer events among tetrapods, provide evidence for a previously hypothesized transoceanic movement of SPIN transposons during the Cenozoic, and further underscore the role of HT in the evolution of vertebrate genomes.
Highlights
Horizontal transfer (HT) is the passage of genetic material between reproductively isolated organisms
We extended these searches to the sequence of ten tuatara bacterial artificial chromosome (BAC) clones produced by the NIH Intramural Sequencing Center and representing a total of 1.6 Mb
This distribution implies that SPIN was transferred independently at least 13 times during the evolution of squamates, which triples the number of HT events of SPIN previously reported among diverse metazoans (Pace et al 2008; Gilbert et al 2010; Novick et al 2010)
Summary
Horizontal transfer (HT) is the passage of genetic material between reproductively isolated organisms. TEs are segments of DNA that are able to move between different genomic loci, often duplicating themselves in the process (Craig et al 2002). Two properties of these elements suggest that they may be more likely than genes to transfer horizontally between organisms: they are capable of mobility and they often represent the single most abundant component of eukaryotic genomes—for example, TEs make up ;45% and ;85% of the human and maize genomes, respectively (Lander et al 2001; Schnable et al 2009)
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