Trends in Ecology & Evolution
ReviewPromiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution
Section snippets
The importance of horizontal transfer of DNA in genome evolution
Horizontal transfer has long been recognized as a crucial mechanism driving bacterial evolution [1]. In contrast, the evolutionary significance of horizontal transfer between the nuclear genomes of multicellular eukaryotes has remained more obscure [2]. We believe this gap in perceived importance is attributable to the disproportionate attention given to the transfer of genes as opposed to non-genic DNA. A fundamental difference in the genomic composition of multicellular eukaryotes compared to
The role of horizontal transfer in the persistence of transposable elements
The question of how TEs and other forms of ‘selfish DNA’ [9] persist in genomes while having no direct selective benefit to the host has long intrigued evolutionary biologists (e.g. 10, 11). Several models have been developed to assess the relative effects of transposition and excision rates, negative selection, and population genetic parameters (such as effective population size) on the long-term survival of TEs in the population (e.g. 12, 13). Most of these models aimed to identify conditions
Detecting HTT in the genomic era
Traditionally, three criteria have been used to infer HTT: (i) patchy distribution of the TE within a group of taxa, (ii) high sequence similarity of the TE from different host species which exceeds levels that would be expected given the divergence time of the hosts, and (iii) incongruence of TE and host phylogeny (reviewed by Refs 19, 20). It is, however, important to keep in mind that each of these patterns may also result from other evolutionary processes, such as stochastic loss and/or
Known cases of HTT: the tip of the iceberg?
Data accumulated over the last two decades have shown that both RNA- and DNA-mediated elements have crossed species boundaries on many occasions (Table 1; see also Supplemental Table 1 and references therein). Our survey of the literature reveals 218 convincing cases of HTT; with 103, 97, and 14 cases affecting DNA transposons, LTR retrotransposons, and non-LTR retrotransposons, respectively (Table 1). The apparent difference in the success rate of HTT among TE types may stem from differences
In search of the smoking gun: mechanisms underlying HTT
While the inherent mobility and replication abilities of TEs undoubtedly facilitate excision and integration, the precise mechanisms by which TEs can be transported between organisms, including potential vectors, remain largely mysterious. Successful transfer requires delivery of DNA from donor to host cell (and to the germline for multicellular organisms), followed by integration into the recipient host genome. It has long been established that ‘naked’ DNA and RNA can circulate in animal
Consequences of HTT for eukaryotic evolution
Regardless of the precise mechanism(s) underlying HTT, the accumulation of cases in the literature clearly points to a recurrent phenomenon that may be viewed as an integral facet of the lifecycle of TEs. But does it matter for eukaryotic evolution? It has been argued that biological innovation in multicellular organisms is largely driven by changes in copy number or function of pre-existing genetic material, rather than by the sudden appearance of genes and pathways de novo [66]. Because TEs
Conclusions and Future Directions
Recognizing the prevalence of HTT and its importance for the long-term persistence of many TEs is a major step towards understanding the impact of this phenomenon on the evolution of eukaryotic genomes. Further progress will necessitate systematic, genome-wide scans to identify broad and unbiased patterns of HTT across different types of TEs and taxonomic groups. This effort should lead to a better understanding of the genetic, physiological and ecological factors influencing HTT. In addition,
Acknowledgments
We would like to acknowledge the research conducted on this topic by many colleagues that could not be cited or discussed due to space constraints. We also wish to thank the following for helpful discussions and comments: E.J. Pritham, J. Meik, B. Koskella, and three anonymous reviewers. This work was supported by NSF award 0805546 to SS and NIH grant R01GM77582 to CF.
Glossary
- Autonomous elements
- Transposable elements that encode the proteins necessary to perform a complete transposition reaction on their own, i.e. to move from one genomic locus to another.
- DNA transposons (Class 2)
- Transposable elements that transpose via a DNA intermediate, also often referred to as ‘cut-and-paste’ elements because they excise and integrate elsewhere, unlike retroelements which do not excise.
- LTR elements
- one of two major subclasses of retroelements comprised of several superfamilies
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Cited by (0)
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These authors contributed equally to this review.