Long-Term and Short-Term Evolutionary Impacts of Transposable Elements on<i>Drosophila</i>

Lee, Yuh Chwen G.; Langley, Charles H.

doi:10.1534/genetics.112.145714

Cited by 52 publications

(66 citation statements)

References 135 publications

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“…In the soma, transcripts retain the third intron, producing a truncated, inactive version of the transposase protein; in the germ line, this intron is spliced out, yielding a functional transposase (35). Host genes responsible for alternative splicing of the third intron [P-element somatic inhibitor (Psi), heterogeneous nuclear ribonucleoprotein at 27C (Hrb27C)] are highly conserved between D. melanogaster and D. simulans (36), and so we anticipated that the same pattern of alternative splicing occurs in D. simulans. We therefore analyzed RNA-seq data from the Florida D. simulans flies for evidence of alternative splicing of the third intron (Fig.…”

Section: Significancementioning

confidence: 99%

The recent invasion of natural Drosophila simulans populations by the P-element

Kofler¹,

Hill²,

Nolte³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

113

154

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The P-element is one of the best understood eukaryotic transposable elements. It invaded Drosophila melanogaster populations within a few decades but was thought to be absent from close relatives, including Drosophila simulans. Five decades after the spread in D. melanogaster, we provide evidence that the P-element has also invaded D. simulans. P-elements in D. simulans appear to have been acquired recently from D. melanogaster probably via a single horizontal transfer event. Expression data indicate that the P-element is processed in the germ line of D. simulans, and genomic data show an enrichment of P-element insertions in putative origins of replication, similar to that seen in D. melanogaster. This ongoing spread of the P-element in natural populations provides a unique opportunity to understand the dynamics of transposable element spread and the associated piwi-interacting RNAs defense mechanisms.T he P-element, one of the best understood eukaryotic transposable elements (TEs), was originally discovered as the causal factor for a syndrome of abnormal phenotypes in Drosophila melanogaster. Crosses in which males derived from newly collected strains were mated with females from long established laboratory stocks produced offspring with spontaneous male recombination, high rates of sterility, and malformed gonadsthat is, "hybrid dysgenesis" (1-4). Eventually it was discovered that hybrid dysgenesis was due to the presence of a TE, the P-element (5, 6), which rapidly became the workhorse of Drosophila transgenesis (5, 7-9). Surveys of strains collected over 70 y show that the P-element spread rapidly in natural D. melanogaster populations, between 1950 and 1990 (10-12), and surveys of other Drosophila species revealed that the P-element had been horizontally transferred (HT) from a distantly related species, Drosophila willistoni (13). As there could be a considerable lag time between the initial transmission of a TE and its invasion of worldwide populations, it is unclear exactly when the P-element first entered D. melanogaster. However, the initial HT event likely occurred somewhere between the spread of D. melanogaster populations into the habitat of D. willistoni, around 1800 (14), and the onset of the worldwide invasion of D. melanogaster populations, around 1950 (10). In any case, the P-element had not been found in close relatives of D. melanogaster, including Drosophila simulans (13-18). The failure of the P-element to invade D. simulans is surprising, as both species are cosmopolitan, are mostly sympatric, and share insertions from many TE families via horizontal transfer (19,20). Furthermore, when artificially injected, the P-element can transpose in D. simulans, albeit at a reduced rate (21, 22). Results and DiscussionThe Recent Invasion of D. simulans Populations. Here, we show that the P-element has recently invaded natural D. simulans populations. We sequenced D. simulans collected from South Africa (in 2012) and from Florida (in 2010) as pools (Pool-seq) (23) and analyzed TE insertions in these ...

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Section: Significancementioning

confidence: 99%

The recent invasion of natural Drosophila simulans populations by the P-element

Kofler¹,

Hill²,

Nolte³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

113

154

View full text Add to dashboard Cite

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“…This deleterious side effect, in combination with 38 the deleterious effects of TE insertions suggests TE insertions should be rare in euchromatic 39regions (Charlesworth and Langley 1989;Charlesworth et al 1997;Lee and Langley 2010). 40Within this model, TEs will enter a genome and spread rapidly through a burst of 41 unsuppressed transposition (Kofler et al 2012;Lee and Langley 2012). The TE will be silenced 42 via the piRNA system and regulated so long as piRNAs are produced against the TE (Senti and 43 Brennecke 2010;Blumenstiel 2011).…”

mentioning

confidence: 99%

Transposable element dynamics are consistent across theDrosophilaphylogeny, despite drastically differing content

Hill

2019

Preprint

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1The evolutionary dynamics of transposable elements (TEs) vary across the tree of life and even 2 between closely related species with similar ecologies. In Drosophila, most of the focus on TE 3 dynamics has been completed in Drosophila melanogaster and the overall pattern indicates that 4TEs show an excess of low frequency insertions, consistent with their fitness cost in the genome. 5However, work outside of D. melanogaster, in the species Drosophila algonquin, suggests that 6 this situation may not be universal, even within Drosophila. Here we test whether the pattern 7 observed in D. melanogaster is similar across five Drosophila species that share a common 8 ancestor more than fifty million years ago. We find that, for most TE families and orders, the 9 patterns are broadly conserved between species, suggesting TEs are primarily costly, and dynamics 10 are conserved in orthologous regions of the host genome. These results suggest that most TEs 11 retain similar activities and fitness costs across the Drosophila phylogeny suggesting little 12 evidence of drift in the dynamics of TEs across the phylogeny. 13 Lu and Clark 2010). Using small RNAs transcribed from TE sequences, the 31 piRNA system targets and degrades complementary TE mRNAs and cause heterochromatin 32 formation on similar TE insertions (Obbard et al. 2009;Blumenstiel 2011;Lee 2015; Senti et al. 33 2015). Within this suppression system, the extent of silencing is then dependent on the expression 34 and copy number of TEs, resulting in the copy number regulation seen in Drosophila (Lee and 35 14Langley 2010). However, the piRNA system can cause the propagation of heterochromatic 36 silencing marks around TE insertions, resulting in the silencing of nearby genes and position effect 37 variegation (Lee and Langley 2010; Lee 2015). This deleterious side effect, in combination with 38 the deleterious effects of TE insertions suggests TE insertions should be rare in euchromatic 39regions (Charlesworth and Langley 1989;Charlesworth et al. 1997;Lee and Langley 2010). 40Within this model, TEs will enter a genome and spread rapidly through a burst of 41 unsuppressed transposition (Kofler et al. 2012;Lee and Langley 2012). The TE will be silenced 42 via the piRNA system and regulated so long as piRNAs are produced against the TE (Senti and 43 Brennecke 2010;Blumenstiel 2011). Following this, you should expect larger genomes with fewer 44active TEs, such as mammals, to have higher TE abundances and TE insertion frequency spectra 45 (IFS) showing no skew towards rare insertions as TE insertions are on average, less costly (Figure 461) (Lee and Langley 2012; Hellen and Brookfield 2013a; Lee 2015). While species with higher 47 O'Grady 2006; Clark et al. 2007). The sequenced species, show striking differences between TE 63families and orders, and make up differing proportions of the genome, between 5 and 40% across 64 the tree (Sessegolo et al. 2016). Additionally, the TE content of two species in the D. affinis 65

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“…Although such rapid phenotypic change could imply strong directional selection, population genetic theory has historically suggested that in sexually reproducing eukaryotes, TE repression is only weakly beneficial (Charlesworth and Langley 1986;Nuzhdin 1999;Lee and Langley 2012). Although repressor alleles confer an advantage by reducing the occurrence of new deleterious TE insertions, recombination and independent assortment rapidly separate repressors from the chromosomes that they have protected from TE-induced mutational load (Charlesworth and Langley 1986).…”

Section: Mutation and Selection In The Rapid Evolution Of Host Represmentioning

confidence: 99%

“…To explore the benefits of repressing hybrid dysgenesis, Lee and Langley (2012) examined the strength of selection on a P cytotype-independent repressor of P-element transposition and hybrid dysgenesis during genome invasion with a deterministic model. They observed a sizable selective advantage for the repressor allele (0.6%) when hybrid dysgenesis was common.…”

Section: Mutation and Selection In The Rapid Evolution Of Host Represmentioning

confidence: 99%

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

Kelleher¹

2016

Genetics

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Transposable elements (TEs) are both important drivers of genome evolution and genetic parasites with potentially dramatic consequences for host fitness. The recent explosion of research on regulatory RNAs reveals that small RNA-mediated silencing is a conserved genetic mechanism through which hosts repress TE activity. The invasion of the Drosophila melanogaster genome by P elements, which happened on a historical timescale, represents an incomparable opportunity to understand how small RNAmediated silencing of TEs evolves. Repression of P-element transposition emerged almost concurrently with its invasion. Recent studies suggest that this repression is implemented in part, and perhaps predominantly, by the Piwi-interacting RNA (piRNA) pathway, a small RNA-mediated silencing pathway that regulates TE activity in many metazoan germlines. In this review, I consider the P-element invasion from both a molecular and evolutionary genetic perspective, reconciling classic studies of P-element regulation with the new mechanistic framework provided by the piRNA pathway. I further explore the utility of the P-element invasion as an exemplar of the evolution of piRNA-mediated silencing. In light of the highly-conserved role for piRNAs in regulating TEs, discoveries from this system have taxonomically broad implications for the evolution of repression.

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Long-Term and Short-Term Evolutionary Impacts of Transposable Elements onDrosophila

Cited by 52 publications

References 135 publications

The recent invasion of natural Drosophila simulans populations by the P-element

The recent invasion of natural Drosophila simulans populations by the P-element

Transposable element dynamics are consistent across theDrosophilaphylogeny, despite drastically differing content

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

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