Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution

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194

234

Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.horizontal transfer | transposable elements | insects | genome evolution | biogeography H orizontal transfer (HT) is the transmission of genetic material between organisms through a mechanism other than reproduction. In prokaryotes, HT is pervasive, its mechanisms are well understood, and it is now viewed as one of the main forces shaping genome architecture and evolution (1, 2). In contrast, the study of HT in eukaryotes is less documented, but has been increasingly investigated. The majority of genes horizontally acquired by eukaryotes come from bacteria, but the extent to which these transfers have contributed to eukaryote evolution is still unclear (3, 4). Gene transfers from eukaryote to eukaryote appear to be largely limited to filamentous organisms, such as oomycetes and fungi (5, 6).In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do. HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,[14][15][16]. However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfe...

“…Such differences may explain the overall higher numbers of HTT events of DNA transposons than retrotransposons reported in our study (1,813 vs. 435 transfers; Fig. 2) and others (13,32).…”

Section: Significancementioning

confidence: 43%

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confidence: 99%

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confidence: 99%

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Massive horizontal transfer of transposable elements in insects

Peccoud

Loiseau

Cordaux

et al. 2017

Self Cite

194

234

“…Rare events such as complementation and recombination might restore the capability of the extracellular life cycle; for example, in invertebrates there have been multiple evolutionary transitions from LTR-retrotransposons to retrovirus-like elements by the gaining of a third ORF analogous to env and an assumed shift from retrotransposition to reinfection (30). There also are examples of cross-species transmission by various TEs that lack an obvious mechanism for reinfection (31).…”

Section: Discussionmentioning

confidence: 99%

Env-less endogenous retroviruses are genomic superspreaders

Magiorkinis

Gifford

Katzourakis

et al. 2012

114

118

Endogenous retroviruses (ERVs) differ from typical retroviruses in being inherited through the host germline and therefore are a unique combination of pathogen and selfish genetic element. Some ERV lineages proliferate by infecting germline cells, as do typical retroviruses, whereas others lack the env gene required for virions to enter cells and thus behave like retrotransposons. We wished to know what factors determined the relative abundance of different ERV lineages, so we analyzed ERV loci recovered from 38 mammal genomes by in silico screening. By modeling the relationship between proliferation and replication mechanism in detail within one group, the intracisternal A-type particles (IAPs), and performing simple correlations across all ERV lineages, we show that when ERVs lose the env gene their proliferation within that genome is boosted by a factor of ∼30. We also show that ERV abundance follows the Pareto principle or 20/80 rule, with ∼20% of lineages containing 80% of the loci. This rule is observed in many biological systems, including infectious disease epidemics, where commonly ∼20% of the infected individuals are responsible for 80% of onward infection. We thus borrow simple epidemiological and ecological models and show that retrotransposition and loss of env is the trait that leads endogenous retroviruses to becoming genomic superspreaders that take over a significant proportion of their host's genome. E ndogenous retroviruses (ERVs) proliferate by the repeated integration of new viral sequences into their host's germline (1), integrations which can become fixed in the host population and have led to ERV sequences (loci) comprising 8-10% of the human and mouse genomes (2, 3) (this number also includes nonautonomous LTR-retrotransposons, which we do not analyze here). These loci form phylogenetically distinct lineages traditionally called "families" (4) (unrelated to the general use of this term in taxonomy), each of which is the result of the expansion of a founder infection of the organism's germline that can have occurred more than ∼100 million years ago (5).ERVs can replicate both as transposable elements (TEs) and viruses. Some lineages copy by an entirely intracellular mechanism and are functionally indistinguishable from the class of TEs called LTR-retrotransposons, whereas others copy within the host germline using cell reinfection in the same manner as the copying within somatic cells of exogenous retroviruses (XRVs) (6). We refer to these replication mechanisms as "retrotransposition" and "reinfection," respectively. Whether an ERV is reinfecting or retrotransposing can be determined by the integrity of its env gene, which produces the protein on the surface of the viral particle that is responsible for cell entry. We can assume that an ERV lineage with a functional env is reinfecting, whereas an ERV lineage with a disintegrated env is retrotransposing (whether reinfection can include germline cells in other host individuals of the same or other species is not known). Some retroviruses w...

“…As a result, TEs and other repetitive DNA can be major determinants of genome size within taxa (27). TEs also vary considerably in the taxonomic breadth of their distribution (28,29). Around 10 different DNA TE superfamilies are currently recognized (28), and many show a broad host taxonomic distribution and signature of lateral transfer between taxa.…”

Section: Types Of Sges and Their Consequencesmentioning

confidence: 99%

Selfish genetic elements, genetic conflict, and evolutionary innovation

Werren

2011

371

Genomes are vulnerable to selfish genetic elements (SGEs), which enhance their own transmission relative to the rest of an individual's genome but are neutral or harmful to the individual as a whole. As a result, genetic conflict occurs between SGEs and other genetic elements in the genome. There is growing evidence that SGEs, and the resulting genetic conflict, are an important motor for evolutionary change and innovation. In this review, the kinds of SGEs and their evolutionary consequences are described, including how these elements shape basic biological features, such as genome structure and gene regulation, evolution of new genes, origin of new species, and mechanisms of sex determination and development. The dynamics of SGEs are also considered, including possible "evolutionary functions" of SGEs.