Wake up of transposable elements following Drosophila simulans worldwide colonization.

Transposable elements (TEs) make up around 10%-15% of the Drosophila melanogaster genome, but its sibling species Drosophila simulans carries only one third as many such repeat sequences. We do not, however, have an overall view of copy numbers of the various classes of TEs (long terminal repeat [LTR] retrotransposons, non-LTR retrotransposons, and transposons) in genomes of natural populations of both species. We analyzed 34 elements in individuals from various natural populations of these species. We show that D. melanogaster has higher average chromosomal insertion site numbers per genome than D. simulans for all TEs except five. The LTR retrotransposons gypsy, ZAM, and 1731 and the transposon bari-1 present similar low copy numbers in both species. The transposon hobo has a large number of insertion sites, with significantly more sites in D. simulans. High variation between populations in number of insertion sites of some elements of D. simulans suggests that these elements can invade the genome of the entire species starting from a local population. We propose that TEs in the D. simulans genome are being awakened and amplified as they had been a long time ago in D. melanogaster.     

Distribution of transposable elements in Drosophila species

We present a global analysis of the distribution of 43 transposable elements (TEs) in 228 species of the Drosophila genus from our data and data from the literature. Data on chromosome localization come from in situ hybridization and presence/absence of the elements from southern analyses. This analysis shows great differences between TE distributions, even among closely related species. Some TEs are distributed according to the phylogeny of their host specie; others do not entirely follow the phylogeny, suggesting horizontal transfers. A higher number of insertion sites for most TEs in the genome of D. melanogaster is observed when compared with that in D. simulans. This suggests either intrinsic differences in genomic characteristics between the two species, or the influence of differing effective population sizes, although biases due to the use of TE probes coming mostly from D. melanogaster and to the way TEs are initially detected in species cannot be ruled out. Data on TEs more specific to the species under consideration are necessary for a better understanding of their distribution in organisms and populations. This revised version was published online in July 2006 with corrections to the Cover Date.     

Evolution of genome size in Drosophila. is the invader's genome being invaded by transposable elements?

Genome size varies considerably between species, and transposable elements (TEs) are known to play an important role in this variability. However, it is far from clear whether TEs are involved in genome size differences between populations within a given species. We show here that in Drosophila melanogaster and Drosophila simulans the size of the genome varies among populations and is correlated with the TE copy number on the chromosome arms. The TEs embedded within the heterochromatin do not seem to be involved directly in this phenomenon, although they may contribute to differences in genome size. Furthermore, genome size and TE content variations parallel the worldwide colonization of D. melanogaster species. No such relationship exists for the more recently dispersed D. simulans species, which indicates that a quantitative increase in the TEs in local populations and fly migration are sufficient to account for the increase in genome size, with no need for an adaptation hypothesis.     

Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes

Transposable elements (TEs) are indwelling components of genomes, and their dynamics have been a driving force in genome evolution. Although we now have more information concerning their amounts and characteristics in various organisms, we still have little data from overall comparisons of their sequences in very closely-related species. While the Drosophila melanogaster genome has been extensively studied, we have only limited knowledge regarding the precise TE sequences in the genomes of the related species Drosophila simulans, Drosophila sechellia and Drosophila yakuba. In this study we analyzed the number and structure of TE copies in the sequenced genomes of these four species. Our findings show that, unexpectedly, the number of TE insertions in D. simulans is greater than that in D. melanogaster, but that most of the copies in D. simulans are degraded and in small fragments, as in D. sechellia and D. yakuba. This suggests that all three species were invaded by numerous TEs a long time ago, but have since regulated their activity, as the present TE copies are degraded, with very few full-length elements. In contrast, in D. melanogaster, a recent activation of TEs has resulted in a large number of almost-identical TE copies. We have detected variants of some TEs in D. simulans and D. sechellia, that are almost identical to the reference TE sequences in D. melanogaster, suggesting that D. melanogaster has recently been invaded by active TE variants from the other species. Our results indicate that the three species D. simulans, D. sechellia, and D. yakuba seem to be at a different stage of their TE life cycle when compared to D. melanogaster. Moreover, we show that D. melanogaster has been invaded by active TE variants for several TE families likely to come from D. simulans or the ancestor of D. simulans and D. sechellia. The numerous horizontal transfer events implied to explain these results could indicate introgression events between these species.     

High rate of recent transposable element-induced adaptation in Drosophila melanogaster

Although transposable elements (TEs) are known to be potent sources of mutation, their contribution to the generation of recent adaptive changes has never been systematically assessed. In this work, we conduct a genome-wide screen for adaptive TE insertions in Drosophila melanogaster that have taken place during or after the spread of this species out of Africa. We determine population frequencies of 902 of the 1,572 TEs in Release 3 of the D. melanogaster genome and identify a set of 13 putatively adaptive TEs. These 13 TEs increased in population frequency sharply after the spread out of Africa. We argue that many of these TEs are in fact adaptive by demonstrating that the regions flanking five of these TEs display signatures of partial selective sweeps. Furthermore, we show that eight out of the 13 putatively adaptive elements show population frequency heterogeneity consistent with these elements playing a role in adaptation to temperate climates. We conclude that TEs have contributed considerably to recent adaptive evolution (one TE-induced adaptation every 200-1,250 y). The majority of these adaptive insertions are likely to be involved in regulatory changes. Our results also suggest that TE-induced adaptations arise more often from standing variants than from new mutations. Such a high rate of TE-induced adaptation is inconsistent with the number of fixed TEs in the D. melanogaster genome, and we discuss possible explanations for this discrepancy.     

Transposable Element Dynamics in Two Sibling Species: Drosophila Melanogaster and Drosophila Simulans

Transposable elements (TEs) in the two sibling species, Drosophila melanogaster and D. simulans, differ considerably in amount and dynamics, with D. simulans having a smaller amount of TEs than D. melanogaster. Several hypotheses have been proposed to explain these differences, based on the evolutionary history of the two species, and claim differences either in the effective size of the population or in genome characteristics. Recent data suggest, however, that the higher amount of TEs in D. melanogaster could be associated with the worldwide invasion of D. melanogaster a long time ago while D. simulans is still under the process of such geographical spread. Stresses due to new environmental conditions and crosses between migrating populations could explain the mobilization of TEs while the flies colonize. Colonization and TE mobilization may be strong evolutionary forces that have shaped and are still shaping the eukaryote genomes.     

A Snapshot of Histone Modifications within Transposable Elements in Drosophila Wild Type Strains

Transposable elements (TEs) are a major source of genetic variability in genomes, creating genetic novelty and driving genome evolution. Analysis of sequenced genomes has revealed considerable diversity in TE families, copy number, and localization between different, closely related species. For instance, although the twin species Drosophila melanogaster and D. simulans share the same TE families, they display different amounts of TEs. Furthermore, previous analyses of wild type derived strains of D. simulans have revealed high polymorphism regarding TE copy number within this species. Several factors may influence the diversity and abundance of TEs in a genome, including molecular mechanisms such as epigenetic factors, which could be a source of variation in TE success. In this paper, we present the first analysis of the epigenetic status of four TE families (roo, tirant, 412 and F) in seven wild type strains of D. melanogaster and D. simulans. Our data shows intra- and inter-specific variations in the histone marks that adorn TE copies. Our results demonstrate that the chromatin state of common TEs varies among TE families, between closely related species and also between wild type strains.     

Population genomics of transposable elements in Drosophila melanogaster

Transposable elements (TEs) are the primary contributors to the genome bulk in many organisms and are major players in genome evolution. A clear and thorough understanding of the population dynamics of TEs is therefore essential for full comprehension of the eukaryotic genome evolution and function. Although TEs in Drosophila melanogaster have received much attention, population dynamics of most TE families in this species remains entirely unexplored. It is not clear whether the same population processes can account for the population behaviors of all TEs in Drosophila or whether, as has been suggested previously, different orders behave according to very different rules. In this work, we analyzed population frequencies for a large number of individual TEs (755 TEs) in five North American and one sub-Saharan African D. melanogaster populations (75 strains in total). These TEs have been annotated in the reference D. melanogaster euchromatic genome and have been sampled from all three major orders (non-LTR, LTR, and TIR) and from all families with more than 20 TE copies (55 families in total). We find strong evidence that TEs in Drosophila across all orders and families are subject to purifying selection at the level of ectopic recombination. We showed that strength of this selection varies predictably with recombination rate, length of individual TEs, and copy number and length of other TEs in the same family. Importantly, these rules do not appear to vary across orders. Finally, we built a statistical model that considered only individual TE-level (such as the TE length) and family-level properties (such as the copy number) and were able to explain more than 40% of the variation in TE frequencies in D. melanogaster.     

Fixation of transposable elements in the Drosophila melanogaster genome

We have investigated at the molecular level four cases in which D. melanogaster middle repetitive DNA probes consistently hybridized to a particular band on chromosomes sampled from a D. melanogaster natural population. Two corresponded to true fixations of a roo and a Stalker element, and the others were artefacts of the in situ hybridization technique caused by the presence of genomic DNA flanking the transposable elements (TEs) in the probes. The two fixed elements are located in the beta-heterochromatin (20A and 80B, respectively) and are embedded in large clusters of other elements, many of which may also be fixed. We also found evidence that this accumulation is an ongoing process. These results support the hypothesis that TEs accumulate in the non-recombining part of the genome. Their implications for the effects of TEs on determining the chromatin structure of the host genomes are discussed in the light of recent evidence for the role of TE-derived small interfering-RNAs as cis -acting determinants of heterochromatin formation.     

Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes

The techniques that are usually used to detect transposable elements (TEs) in nucleic acid sequences rely on sequence similarity with previously characterized elements. However, these methods are likely to miss many elements in various organisms. We tested two strategies for the detection of unknown elements. The first, which we call "TBLASTX strategy," searches for TE sequences by comparing the six-frame translations of the nucleic acid sequences of known TEs with the genomic sequence of interest. The second, "repeat-based strategy," searches genomic sequences for long repeats and clusters them in groups of similar sequences. TE copies from a given family are expected to cluster together. We tested the Drosophila melanogaster genomic sequence and the recently sequenced Anopheles gambiae genome in which most TEs remain unknown. We showed that the "TBLASTX strategy" is very efficient as it detected at least 332 new TE families in D. melanogaster and 400 in A. gambiae. This was unexpected in Drosophila as TEs of this organism have been extensively studied. The "repeat-based strategy" appeared to be very inefficient because of two problems: (i) TE copies are heavily deleted and few copies share homologous regions, and (ii) segmental duplications are frequent and it is not easy to distinguish them from TE copies.     

Constitutive heterochromatin and transposable elements in Drosophila melanogaster

Several families of transposable elements (TEs), most of them belonging to the retrotransposon catagory, are particularly enriched in Drosophila melanogaster constitutive heterochromatin. The enrichment of TE-homologous sequences into heterochromatin is not a peculiar feature of the Drosophila genome, but appears to be widespread among higher eukaryotes. The constitutive heterochromatin of D. melanogaster contains several genetically active domains; this raises the possibility that TE-homologous sequences inserted into functional heterochromatin compartments may be expressed. In this review, I present available data on the genetic and molecular organization of D. melanogaster constitutive heterochromatin and its relationship with transposable elements. The implications of these findings on the possible impact of heterochromatic TEs on the function and evolution of the host genome are also discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

Combined evidence annotation of transposable elements in genome sequences

Transposable elements (TEs) are mobile, repetitive sequences that make up significant fractions of metazoan genomes. Despite their near ubiquity and importance in genome and chromosome biology, most efforts to annotate TEs in genome sequences rely on the results of a single computational program, RepeatMasker. In contrast, recent advances in gene annotation indicate that high-quality gene models can be produced from combining multiple independent sources of computational evidence. To elevate the quality of TE annotations to a level comparable to that of gene models, we have developed a combined evidence-model TE annotation pipeline, analogous to systems used for gene annotation, by integrating results from multiple homology-based and de novo TE identification methods. As proof of principle, we have annotated "TE models" in Drosophila melanogaster Release 4 genomic sequences using the combined computational evidence derived from RepeatMasker, BLASTER, TBLASTX, all-by-all BLASTN, RECON, TE-HMM and the previous Release 3.1 annotation. Our system is designed for use with the Apollo genome annotation tool, allowing automatic results to be curated manually to produce reliable annotations. The euchromatic TE fraction of D. melanogaster is now estimated at 5.3% (cf. 3.86% in Release 3.1), and we found a substantially higher number of TEs (n = 6,013) than previously identified (n = 1,572). Most of the new TEs derive from small fragments of a few hundred nucleotides long and highly abundant families not previously annotated (e.g., INE-1). We also estimated that 518 TE copies (8.6%) are inserted into at least one other TE, forming a nest of elements. The pipeline allows rapid and thorough annotation of even the most complex TE models, including highly deleted and/or nested elements such as those often found in heterochromatic sequences. Our pipeline can be easily adapted to other genome sequences, such as those of the D. melanogaster heterochromatin or other species in the genus Drosophila.     

Patterns of transposable element variation and clinality in Drosophila

Natural populations often exist in spatially diverse environments and may experience variation in the strength and targets of natural selection across their ranges. Drosophila provides an excellent opportunity to study the effects of spatially varying selection in natural populations, as both Drosophila melanogaster and Drosophila simulans live across a wide range of environments in North America. Here, we characterize patterns of variation in transposable elements (TEs) from six populations of D. melanogaster and nine populations of D. simulans sampled from multiple latitudes across North America. We find a nearly twofold excess of TEs in D. melanogaster relative to D. simulans, with this difference largely driven by TEs segregating at the lowest and highest allele frequencies. We find no effect of latitude on either total TE abundance or average TE allele frequencies in either species. Moreover, we show that, as a class of mutations, the most common patterns of TE variation do not coincide with the sampled latitudinal gradient, nor are they consistent with local adaptation acting on environmental differences found in the most extreme latitudes. We also do not find a cline in ancestry for North American D. melanogaster—for either TEs or single nucleotide polymorphisms—suggesting a limited role for demography in shaping patterns of TE variation. Though we find little evidence for widespread clinality among TEs in Drosophila, this does not necessarily imply a limited role for TEs in adaptation. We discuss the need for improved models of adaptation to large‐scale environmental heterogeneity, and how these might be applied to TEs.     

Codon Usage by Transposable Elements and Their Host Genes in Five Species

We compared the codon usage of sequences of transposable elements (TEs) with that of host genes from the species Drosophila melanogaster, Arabidopsis thaliana, Caenorhabditis elegans, Saccharomyces cerevisiae, and Homo sapiens. Factorial correspondence analysis showed that, regardless of the base composition of the genome, the TEs differed from the genes of their host species by their AT-richness. In all species, the percentage of A + T on the third codon position of the TEs was higher than that on the first codon position and lower than that in the noncoding DNA of the genomes. This indicates that the codon choice is not simply the outcome of mutational bias but is also subject to selection constraints. A tendency toward higher A + T on the third position than on the first position was also found in the host genes of A. thaliana, C. elegans, and S. cerevisiae but not in those of D. melanogaster and H. sapiens. This strongly suggests that the AT choice is a host-independent characteristic common to all TEs. The codon usage of TEs generally appeared to be different from the mean of the host genes. In the AT-rich genomes of Arabidopsis thaliana, Caenorhabditis elegans, and Saccharomyces cerevisiae, the codon usage bias of TEs was similar to that of weakly expressed genes. In the GC-rich genome of D. melanogaster, however, the bias in codon usage of the TEs clearly differed from that of weakly expressed genes. These findings suggest that selection acts on TEs and that TEs may display specific behavior within the host genomes. Received: 2 May 2001 / Accepted: 29 October 2001     

Evolution of the Transposable Element Mariner in Drosophila Species

The distribution of the transposable element mariner was examined in the genus Drosophila. Among the eight species comprising the melanogaster species subgroup, the element is present in D. mauritiana, D. simulans, D. sechellia, D. yakuba and D. teissieri, but it is absent in D. melanogaster, D. erecta and D. orena. Multiple copies of mariner were sequenced from each species in which the element occurs. The inferred phylogeny of the elements and the pattern of divergence were examined in order to evaluate whether horizontal transfer among species or stochastic loss could better account for the discontinuous distribution of the element among the species. The data suggest that the element was present in the ancestral species before the melanogaster subgroup diverged and was lost in the lineage leading to D. melanogaster and the lineage leading to D. erecta and D. orena. This inference is consistent with the finding that mariner also occurs in members of several other species subgroups within the overall melanogaster species group. Within the melanogaster species subgroup, the average divergence of mariner copies between species was lower than the coding region of the alcohol dehydrogenase (Adh) gene. However, the divergence of mariner elements within species was as great as that observed for Adh. We conclude that the relative sequence homogeneity of mariner elements within species is more likely a result of rapid amplification of a few ancestral elements than of concerted evolution. The mariner element may also have had unequal mutation rates in different lineages.     

New regulatory regions of Drosophila 412 retrotransposable element generated by recombination

There are no doubts that transposable elements (TEs) have greatly influenced genomes evolution. They have, however, evolved in different ways throughout mammals, plants, and invertebrates. In mammals they have been shown to be widely present but with low transposition activity; in plants they are responsible for large increases in genome size. In Drosophila, despite their low amount, transposition seems to be higher. Therefore, to understand how these elements have evolved in different genomes and how host genomes have proposed to go around them, are major questions on genome evolution. We analyzed sequences of the retrotransposable elements 412 in natural populations of the Drosophila simulans and D. melanogaster species that greatly differ in their amount of TEs. We identified new subfamilies of this element that were the result of mutation or insertion-deletion process, but also of interfamily recombinations. These new elements were well conserved in the D. simulans natural populations. The new regulatory regions produced by recombination could give rise to new elements able to overcome host control of transposition and, thus, become potential genome invaders.     

Is genome size influenced by colonization of new environments in dipteran species?

Genome size differences are usually attributed to the amplification and deletion of various repeated DNA sequences, including transposable elements (TEs). Because environmental changes may promote modifications in the amount of these repeated sequences, it has been postulated that when a species colonizes new environments this could be followed by an increase in its genome size. We tested this hypothesis by estimating the genome size of geographically distinct populations of Drosophila ananassae, Drosophila malerkotliana, Drosophila melanogaster, Drosophila simulans, Drosophila subobscura, and Zaprionus indianus, all of which have known colonization capacities. There was no strong statistical differences between continents for most species. However, we found that populations of D. melanogaster from east Africa have smaller genomes than more recent populations. For species in which colonization is a recent event, the differences between genome sizes do not thus seem to be related to colonization history. These findings suggest either that genome size is seldom modified in a significant way during colonization or that it takes time for genome size of invading species to change significantly.