The P-element strikes again: the recent invasion of naturalDrosophila simulanspopulations

The P-element is one of the best understood eukaryotic transposable elements. It invadedDrosophila melanogasterpopulations within a few decades, but was thought to be absent from close relatives, includingD. simulans. Five decades after the spread inD. melanogaster, we provide evidence that the P-element has also invadedD. simulans. P-elements inD. simulansappear to have been acquired recently fromD. melanogasterprobably via a single horizontal transfer event. Expression data indicate that the P-element is processed in the germline ofD. simulans, and genomic data show an enrichment of P-element insertions in putative origins of replication, similar to that seen inD. melanogaster. This ongoing spread of the P-element in natural populations provides an unique opportunity to understand the dynamics of transposable element spreads and the associated piRNA defense mechanisms.

Download Full-text

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1500758112 ◽

2015 ◽

Vol 112 (21) ◽

pp. 6659-6663 ◽

Cited By ~ 65

Author(s):

Robert Kofler ◽

Tom Hill ◽

Viola Nolte ◽

Andrea J. Betancourt ◽

Christian Schlötterer

Keyword(s):

Defense Mechanisms ◽

Germ Line ◽

Natural Populations ◽

Genomic Data ◽

Drosophila Simulans ◽

P Element ◽

Expression Data ◽

Transfer Event ◽

P Elements ◽

Close Relatives

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.

Download Full-text

The Regulatory Properties of Autonomous Subtelomeric P Elements Are Sensitive to a Suppressor of variegation in Drosophila melanogaster

Genetics ◽

10.1093/genetics/143.4.1663 ◽

1996 ◽

Vol 143 (4) ◽

pp. 1663-1674 ◽

Cited By ~ 3

Author(s):

Stéphane Ronsseray ◽

Monique Lehmann ◽

Danielle Nouaud ◽

Dominique Anxolabéhère

Keyword(s):

Drosophila Melanogaster ◽

Genetic Recombination ◽

Natural Populations ◽

P Element ◽

Single Element ◽

Heterochromatin Protein 1 ◽

X Chromosomes ◽

P Elements ◽

Associated Sequences ◽

Regulatory Properties

Abstract Genetic recombination was used in Drosophila melanogaster to isolate P elements, inserted at the telomeres of X chromosomes (cytological site 1A) from natural populations, in a genetic background devoid of other P elements. We show that complete maternally inherited P repression in the germline (P cytotype) can be elicited by only two autonomous P elements at 1A and that a single element at this site has partial regulatory properties. The analysis of the surrounding chromosomal regions of the P elements at 1A shows that in all cases these elements are flanked by Telomeric Associated Sequences, tandemly repetitive noncoding sequences that have properties of heterochromatin. In addition, we show that the regulatory properties of P elements at 1A can be inhibited by some of the mutant alleles of the Su(var)205 gene and by a deficiency of this gene. However, the regulatory properties of reference P strains (Harwich and Texas 007) are not impaired by Su(var)205 mutations. Su(var)205 encodes Heterochromatin Protein 1 (HP1). These results suggest that the HP1 dosage effect on the P element properties is sitedependent and could involve the structure of the chromatin.

Download Full-text

Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300030111 ◽

1992 ◽

Vol 59 (1) ◽

pp. 1-9 ◽

Cited By ~ 27

Author(s):

Walter F. Eanes ◽

Cedric Wesley ◽

Brian Charlesworth

Keyword(s):

Mathematical Model ◽

Drosophila Melanogaster ◽

Copy Number ◽

Natural Populations ◽

P Element ◽

P Elements ◽

Chromosomal Inversions ◽

Associated Production ◽

African Populations ◽

Parameter Values

SummaryThe accumulation of a transposable element inside chromosomal inversions is examined theoretically by a mathematical model, and empirically by counts of P elements associated with inversion polymorphisms in natural populations of Drosophila melanogaster. The model demonstrates that, if heterozygosity for an inversion effectively reduces element associated production of detrimental chromosome rearrangements, a differential accumulation of elements is expected, with increased copy number inside the minority inversion. Several-fold differential accumulations are possible with certain parameter values. We present data on P element counts for inversion polymorphisms on all five chromosome arms of 157 haploid genomes from two African populations. Our observations show significantly increased numbers of elements within the regions associated with the least common, or minority arrangements, in natural inversion polymorphisms.

Download Full-text

Transposable element-induced fitness mutations in Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300024794 ◽

1986 ◽

Vol 48 (2) ◽

pp. 77-87 ◽

Cited By ~ 50

Author(s):

Trudy F. C. Mackay

Keyword(s):

Drosophila Melanogaster ◽

Extraction Procedure ◽

Natural Populations ◽

P Element ◽

Recessive Lethal ◽

P Elements ◽

Fitness Traits ◽

Mutational Effect ◽

Evolution Of Transposable Elements ◽

Mutational Variance

SummaryP element mutagenesis was used to contaminate M strain second chromosomes with P elements. The contaminated lines were compared to uncontaminated control lines for homozygous and heterozygous fitness and its components. Mean homozygous fitness, viability and fertility of chromosome lines contaminated with P elements is decreased relative to the uncontaminated control lines by, respectively, 55, 28 and 40%. Variance among contaminated homozygous lines of total fitness increases by a factor of 1·5, variance of viability by a factor of 5·9, and variance of fertility by a factor of 1·9, compared to variance of these traits among the population of uncontaminated homozygous chromosomes. Estimates of P-element-induced mutational variance among second chromosome lines for homozygous fitness, viability and fertility are, respectively, 2 × 10−2, 5 × 10−2 and 2 × 10−2. This magnitude of mutational effect is equivalent, in terms of incidence of induced recessive lethal chromosomes and D:L ratio, to a dose of approximately 1·0–2·5 × 10−3 m EMS. The distributions of fitness traits among M-derived second chromosome homozygous lines contaminated with P elements are remarkably similar in many regards to distributions of fitness and viability of chromosomal homozygotes derived from natural Drosophila populations. It is possible that a proportion of the fitness variation previously observed (reviewed by Simmons & Crow, 1977) following homozygosis of wild chromosomes was not present in the natural populations, but was generated by P-element transposition during the chromosome extraction procedure. P-element-induced fitness mutations appear to be completely recessive. Implications for models of evolution of transposable elements are discussed.

Download Full-text

Disgenesia do híbrido em populações naturais de Drosophila melanogaster.

Ciência e Natura ◽

10.5902/2179460x27019 ◽

1999 ◽

Vol 21 (21) ◽

pp. 51 ◽

Cited By ~ 1

Author(s):

Chirlei Cintia Klein ◽

Liliana Essi ◽

Ronaldo Medeiros Golombieski ◽

Élgion Lúcio da Silva Loreto

Keyword(s):

Drosophila Melanogaster ◽

Molecular Analysis ◽

Natural Populations ◽

Rio Grande ◽

P Element ◽

Rio Grande Do Sul ◽

Genetic Traits ◽

P Elements ◽

Regulatory Capacity ◽

Element Activity

Hybrid dysgenesis has been defined as a remarkable syndrome of correlated genetic traits that are produced in some particular crosses between certain strains. The present study main objective was classify recently collected Drosophila melanogaster strains in relation to P element activity and regulatory capacity. Our results to natural populations trapped from Rio Grande do Sul, Brazil and Colombia shows that it fell on Q class, since all examinated strains has showed P elements by molecular analysis and low P activity. In the same way, these strains shows low susceptibility to P element action. The bigger values found in the colombian population are in agreement with the clinal hypothesis to P element activity.

Download Full-text

Evidence for horizontal transmission of the P transposable element between Drosophila species.

Genetics ◽

10.1093/genetics/124.2.339 ◽

1990 ◽

Vol 124 (2) ◽

pp. 339-355 ◽

Cited By ~ 12

Author(s):

S B Daniels ◽

K R Peterson ◽

L D Strausbaugh ◽

M G Kidwell ◽

A Chovnick

Keyword(s):

Horizontal Transfer ◽

Horizontal Transmission ◽

Natural Populations ◽

P Element ◽

Base Substitution ◽

Potential Donor ◽

Transfer Event ◽

P Elements ◽

Autonomous Element ◽

Group A

Abstract Several studies have suggested that P elements have rapidly spread through natural populations of Drosophila melanogaster within the last four decades. This observation, together with the observation that P elements are absent in the other species of the melanogaster subgroup, has lead to the suggestion that P elements may have entered the D. melanogaster genome by horizontal transmission from some more distantly related species. In an effort to identify the potential donor in the horizontal transfer event, we have undertaken an extensive survey of the genus Drosophila using Southern blot analysis. The results showed that P-homologous sequences are essentially confined to the subgenus Sophophora. The strongest P hybridization occurs in species from the closely related willistoni group. A wild-derived strain of D. willistoni was subsequently selected for a more comprehensive molecular examination. As part of the analysis, a complete P element was cloned and sequenced from this line. Its nucleotide sequence was found to be identical to the D. melanogaster canonical P, with the exception of a single base substitution at position 32. When the cloned element was injected into D. melanogaster embryos, it was able to both promote transposition of a coinjected marked transposon and induce singed-weak mutability, thus demonstrating its ability to function as an autonomous element. The results of this study suggest that D. willistoni may have served as the donor species in the horizontal transfer of P elements to D. melanogaster.

Download Full-text

Transposable element-induced polygenic mutations in Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300027117 ◽

1987 ◽

Vol 49 (3) ◽

pp. 225-233 ◽

Cited By ~ 19

Author(s):

Trudy F. C. Mackay

Keyword(s):

Drosophila Melanogaster ◽

Transposable Element ◽

Quantitative Traits ◽

Natural Populations ◽

P Element ◽

Environmental Variance ◽

X Ray ◽

P Elements ◽

Very High ◽

Mutational Variance

SummaryP-element mutagenesis was used to contaminate M-strain second chromosomes with P elements. The effect of P-element transposition on abdominal and sternopleural bristle scores and on female productivity was deduced by comparing the distributions of these quantitative traits among the contaminated second-chromosome lines with a control population of M-strain second-chromosome lines free of P elements. Estimates of P-element-induced mutational variance, Vm, for these characters are very high, and mutational ‘heritabilities’ (Vm/Ve, the ratio of mutational variance to environmental variance) are of the same order as heritabilities of these traits from natural populations. P-element-induced mutational variance of abdominal bristle score is roughly two orders of magnitude greater than spontaneous and X-ray-induced Vm/Ve for this trait.

Download Full-text

Hybrid dysgenesis in Drosophila melanogaster: the elimination of P elements through repeated backcrossing to an M-type strain

Genome ◽

10.1139/g87-033 ◽

1987 ◽

Vol 29 (1) ◽

pp. 195-200 ◽

Cited By ~ 2

Author(s):

Allen G. Good ◽

Donal A. Hickey

Keyword(s):

Drosophila Melanogaster ◽

Dna Hybridization ◽

Copy Number ◽

Natural Populations ◽

Hybrid Dysgenesis ◽

P Element ◽

P Elements ◽

Element Activity ◽

Equivalent Reduction ◽

Replicative Transposition

The rapid increase in the frequency of P elements in natural populations of Drosophila melanogaster has led to the suggestion that these elements can spread in nature through replicative transposition. In an attempt to model the introduction of a small number of P flies into an M population we backcrossed P flies and their offspring to M flies. Two components of dysgenesis, P element activity and P element copy number (measured by DNA hybridization), were monitored each generation. In these experiments P elements were not capable of spreading rapidly enough to maintain 30–50 copies per fly and were rapidly lost from the population. We also found that the reduction in a fly's ability to induce gonadal dysgenesis was matched by an equivalent reduction in P element copy number as measured by DNA hybridization. These results are discussed in terms of the conventional mechanisms of selection or segregation; the conclusion is that there are conditions under which P elements can be lost from a population. Key words: hybrid dysgenesis, P element, transposable elements, Drosophila.

Download Full-text

Rapid spread of transposable p elements in experimental populations of Drosophila melanogaster.

Genetics ◽

10.1093/genetics/122.2.387 ◽

1989 ◽

Vol 122 (2) ◽

pp. 387-396 ◽

Cited By ~ 3

Author(s):

A G Good ◽

G A Meister ◽

H W Brock ◽

T A Grigliatti ◽

D A Hickey

Keyword(s):

Drosophila Melanogaster ◽

Gonadal Dysgenesis ◽

Natural Populations ◽

P Element ◽

P Elements ◽

Rapid Spread ◽

Laboratory Populations ◽

Experimental Populations

Abstract The invasion of P elements in natural populations of Drosophila melanogaster was modeled by establishing laboratory populations with 1%, 5% and 10% P genomes and monitoring the populations for 20 generations. In one experiment, the ability of flies to either induce or suppress gonadal sterility in different generations was correlated with the amount of P element DNA. In a second experiment, the percentage of genomes that contained P elements, and the distribution of P elements among individual flies was monitored. The ability to induce gonadal dysgenesis increased rapidly each generation. However, the increase in P cytotype lagged behind by five to ten generations. The total amount of P element DNA and the frequency of flies containing P elements increased each generation. The number of P elements within individual genomes decreased initially, but then increased. Finally, the distribution of P elements within the genomes of individuals from later generations varied considerably, and this pattern differed from the parental P strain. These results suggest that the interaction between the assortment and recombination of chromosomal segments, and multiplicative transposition could result in the rapid spread of P elements in natural populations.

Download Full-text

Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/120.4.1003 ◽

1988 ◽

Vol 120 (4) ◽

pp. 1003-1013

Author(s):

M S Jackson ◽

D M Black ◽

G A Dover

Keyword(s):

Drosophila Melanogaster ◽

Copy Number ◽

Natural Populations ◽

Selective Advantage ◽

Complex Interaction ◽

Hybrid Dysgenesis ◽

P Element ◽

Deletion Derivative ◽

P Elements ◽

The Way

Abstract Mobile P elements in Drosophila melanogaster cause hybrid dysgenesis if their mobility is not repressed. One type of repression, termed P cytotype, is a complex interaction between chromosomes carrying P elements and cytoplasm and is transmitted through the cytoplasm only of females. Another type of repression is found in worldwide M' strains that contain approximately 30 copies per individual of one particular P element deletion-derivative termed the KP element. This repression is transmitted equally through both sexes. In the present study we show that biparentally transmitted repression increases in magnitude together with a rapid increase in KP copy-number in genotypes starting with one or a few KP elements and no other deletion-derivatives. Such correlated increases in repression and KP number per genome occur only in the presence of complete P elements, supporting the interpretation that they are probably a consequence of the selective advantage enjoyed by flies carrying the highest numbers of KP elements. Analysis of Q strains also reveals the presence of qualitative differences in the way the repression of dysgenesis is transmitted. In general, Q strains not containing KP elements have the P cytotype mode of repression, whereas Q strains with KP elements transmit repression through both sexes. This difference among Q strains further supports the existence of at least two types of repression of P-induced hybrid dysgenesis in natural populations of D. melanogaster.

Download Full-text