Evidence for recent horizontal transfer of gypsy-homologous LTR-retrotransposon gtwin into Drosophila erecta followed by its amplification with multiple aberrations

Long terminal repeat (LTR) retrotransposon gtwin was initially discovered in silico, and then it was isolated as gypsy-homologous sequence from Drosophila melanogaster strain, G32. The presence of ORF3 suggests, that gtwin, like gypsy, may be an endogenous retrovirus, which can leave the cell and infect another one. Therefore, in this study we decided to investigate the distribution of gtwin in different species of the melanogaster subgroup in order to find out whether gtwin can be transferred horizontally as well as vertically. Gtwin was found in all 9 species of this subgroup, hence it seems to have inhabited the host genomes for a long time. In addition, we have shown that in the Drosophila erecta genome two gtwin families are present. The first one has 93% of identity to D. melanogaster element and is likely to be a descendant of gtwin that existed in Drosophila before the divergence of the melanogaster subgroup species. The other one has >99% of identity to D. melanogaster gtwin. The most reasonable explanation is that this element has been recently horizontally transferred between D. melanogaster and D. erecta. The number and variety of gtwin copies from the "infectious" family suggest that after the horizontal transfer into D. erecta genome, gtwin underwent amplification and aberrations, leading to the rise of its diverse variants.     

Distribution and conservation of sequences homologous to the 1731 retrotransposon in Drosophila

The distribution of 1731 retrotransposon-hybridizing sequences in the family Drosophilidae has been studied using a 1731 probe from Drosophila melanogaster. Squash blot and Southern blot analyses of 42 species reveal that the 1731 sequences are widespread within both the Sophophora and Drosophila subgenera and are also present in the genera Scaptomyza and Zaprionus. Hence the 1731 retrotransposon family appears to have a long evolutionary history in the Drosophilidae genome. Differences of hybridization signal intensity suggested that the 1731 sequence is well conserved only in the three species most closely related to D. melanogaster (D. simulans, D. mauritiana, and D. sechellia). A survey of insertion sites in numerous different populations of the previous four species by in situ hybridization to polytene chromosomes has shown in all cases both chromocentric hybridizations and a low number of sites (0-5) on the chromosomal arms. This number of sites is among the lowest observed in D. melanogaster and D. simulans when 1731 is compared with other retrotransposon families. In addition, we have observed species-specific patterns of the chromocentric hybridization signal, suggesting rapid modifications of the beta-heterochromatin components since the radiation of the melanogaster subgroup.      

Mobile dispersed repeated DNA elements in the Drosophila genome

The molecular and cytogenetic organizations of 19 nonhomologous dispersed repeated sequence families were studied in 15 different laboratory strains of Drosophila melanogaster. Elements from each of the families appear to undergo transposition within the Drosophila genome, because there were striking differences in both the number and chromosomal locations of these elements between strains. A significant fraction (greater than 1%) of Drosophila DNA therefore has an unstable genomic organization. Each middle repetitive family exhibited similar variations in the chromosomal distribution of elements between the strains. Although the movements of these elements are not limited to a small number of genomic sites, there are chromosomal regions where elements from the different dispersed repeated DNA families appear to be clustered. The locations of such preferred integration sites are different in each of the D. melanogaster strains examined.     

Horizontal transfer of hobo transposable elements within the Drosophila melanogaster species complex: evidence from DNA sequencing.

The hobo family of transposable elements, one of three transposable-element families that cause hybrid dysgenesis in Drosophila melanogaster, appears to be present in all members of the D. melanogaster species complex: D. melanogaster, D. simulans, D. mauritiana, and D. sechellia. Some hobo-hybridizing sequences are also found in the other members of the melanogaster subgroup and in many members of the related montium subgroup. Surveys of older isofemale lines of D. melanogaster suggest that complete hobo elements were absent prior to 50 years ago and that hobo has recently been introduced into the species by horizontal transfer. To test the horizontal transfer hypothesis, the 2.6-kb XhoI fragments of hobo elements from D. melanogaster, D. simulans, and D. mauritiana were cloned and sequenced. The DNA sequences reveal an extremely low level of divergence and support the conclusion that the active hobo element has been horizontally transferred into or among these species in the recent past.     

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.     

Wanderings of Hobo: A Transposon in Drosophila Melanogaster and its Close Relatives

The transposon hobo is present in the genomes of Drosophila melanogaster and Drosophila simulans (and D. mauritiana and probably D. sechellia, based on Southern blots) as full-size elements and internally deleted copies. The full-size melanogaster, simulans and mauritiana hobo elements are 99.9% identical at the DNA sequence level, and internally deleted copies in these species essentially differ only in having deletions. In addition to these, hobo-related sequences are present and detectable with a hobo probe in all these species. Those in D. melanogaster are 86-94% identical to the canonical hobo, but with many indels. We have sequenced one that appears to be inserted in heterochromatin (GenBank Acc. No. AF520587). It is 87.6% identical to the canonical hobo, but quite fragmented by indels, with remnants of other transposons inserted in and near it, and clearly is defunct. Numerous similar elements are found in the sequenced D. melanogaster genome. It has recently been shown that some are fixed in the euchromatic genome, but it is probable that still more reside in heterochromatic regions not included in the D. melanogaster genome database. They are probably all relics of an earlier introduction of hobo into the ancestral species. There appear to have been a minimum of two introductions of hobo into the melanogaster subgroup, and more likely three, two ancient and one quite recent. The recent introduction of hobo was probably followed by transfers between the extant species (whether 'horizontally' or by infrequent interspecific hybridization).     

Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements

Horizontal transmission has been well documented as a major mechanism for the dissemination of mariner-like elements (MLEs) among species. Less well understood are mechanisms that limit vertical transmission of MLEs resulting in the "spotty" or discontinuous distribution observed in closely related species. In this article we present evidence that the genome of the common ancestor of the melanogaster species subgroup of Drosophila contained an MLE related to the mellifera (honey bee) subfamily. Horizontal transmission, approximately 3-10 MYA, is strongly suggested by the observation that the sequence of the MLE in Drosophila erecta is 97% identical in nucleotide sequence with that of an MLE in the cat flea, Ctenocephalides felis. The D. erecta MLE has a spotty distribution among species in the melanogaster subgroup. The element has a high copy number in D. erecta and D. orena, a moderate copy number in D. teissieri and D. yakuba, and was apparently lost ("stochastic loss") in the lineage leading to D. melanogaster, D. simulans, D. mauritiana, and D. sechellia. In D. erecta, most copies are concentrated in the heterochromatin. Two copies from D. erecta, denoted De12 and De19, were cloned and sequenced, and they appear to be nonfunctional ("vertical inactivation"). It therefore appears that the predominant mode of MLE evolution is vertical inactivation and stochastic loss balanced against occasional reinvasion of lineages by horizontal transmission.      

Genomic distribution of the retrovirus-like element ZAM in Drosophila

The mobile element ZAM, recently identified in Drosophila melanogaster, is similar in structure and coding potential to vertebrate retroviruses. In this paper, we analyze the insertional and structural polymorphism of this element and show that members of this family appear to have a long evolutionary history in the genome of Drosophila. It is present in all the species of the D. melanogaster subgroup and in more distantly related species like D. takahashii, D. ananassae, or D. virilis but in a lower copy number or with a lower homology. Two categories of strains have been previously identified in D. melanogaster: strains with a high copy number of ZAM and strains with a low copy number. Here, we show that ZAM is at least in a low copy number in each tested strain of the species analyzed. The study of ZAM's genomic distribution by FISH mapping analysis to salivary gland polytene chromosomes or on mitotic chromosomes indicates that most of the insertion sites of ZAM elements are associated with the constitutive heterochromatin regardless of the ZAM copy number. In addition, our results suggest that multiple ZAM elements are present at the insertion sites visualized by in situ experiments. This revised version was published online in August 2006 with corrections to the Cover Date.     

How different are recently diverged species? More than 150 phenotypic differences have been reported for the D. melanogaster species subgroup.

The nine species of the Drosophila melanogaster subgroup are currently one of the best systems for studying the genetic basis of species differences and speciation. However, despite the availability of complete genome sequences from most of these species, no comprehensive accounting of their phenotypic differences has been made. We gathered data from about 200 papers published between 1919 and 2008 that report phenotypic differences between species of the D. melanogaster species subgroup and we compiled 163 morphological, physiological and behavioral traits that differ between at least two species of the D. melanogaster subgroup. Our compilation is available online at www.normalesup.org/~vorgogoz/FlyPhenomics. The FlyPhenomics database provides a useful starting point for Drosophila researchers who aim to identify the mutations underlying phenotypic variation.     

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.     

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.     

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.     

Genomewide comparative analysis of the highly abundant transposable element DINE-1 suggests a recent transpositional burst in Drosophila yakuba

DINE-1 (Drosophila interspersed element) is the most abundant repetitive sequence in the Drosophila genome derived from transposable elements. It comprises >1% of the Drosophila melanogaster genome (DMG) and is believed to be a relic from an ancient transpositional burst that occurred approximately 5-10 MYA. We performed a genomewide comparison of the abundance, sequence variation, and chromosomal distribution of DINE-1 in D. melanogaster and D. yakuba. Unlike the highly diverged copies in the DMG (pairwise distance approximately 15%), DINE-1's in the Drosophila yakuba genome (DYG) have diverged by only 3.4%. Moreover, the chromosomal distribution of DINE-1 in the two species is very different, with a significant number of euchromatic insertions found only in D. yakuba. We propose that these different patterns are caused by a second transpositional burst of DINE-1's in the D. yakuba genome approximately 1.5 MYA. On the basis of the sequence of these recently transposed copies, we conclude that DINE-1 is likely to be a family of nonautomomous DNA transposons. Analysis of the chromosomal distribution of two age groups of DINE-1's in D. yakuba indicates that (1) there is a negative correlation between recombination rates and the density of DINE-1's and (2) younger copies are more evenly distributed in the chromosome arms, while older copies are mostly located near the centromere regions. Our results fit the predictions of a selection-transposition balance model. Our data on whole-genome comparison of a highly abundant TE among Drosophila sibling species demonstrate the unexpectedly dynamic nature of TE activity in different host genomes.     

以ND4L和ND4基因为标记探讨黑腹果蝇种组的系统发育关系

多年来的形态学、染色体组学以及DNA序列几个方面的研究均没有很好地阐明黑腹果蝇种组内的系统发育关系。本实验测定了33个样品的ND4和31个样品的ND4L基因序列,以D．obscuroides为外群,用最大简约法和Bayesian法分别构建进化树。结果表明两种方法构建的拓扑结构一致,而且大部分支系的支持率较高。整个黑腹果蝇种组分成三大谱系：1）montium种亚组;2）ananssae种亚组;3）Oriental种亚组（melanogaster、ficsphila、eugracilis、elegans、suzukii、takahashii）。montium是最早分化的种亚组。在第三谱系中,melanogaster分化得最早;然后依次是ficsphila,eugracilis,elegans;suzukii与takahashii为姐妹种亚组,最后分化。     

Adaptive evolution of recently duplicated accessory gland protein genes in desert Drosophila

The relationship between animal mating system variation and patterns of protein polymorphism and divergence is poorly understood. Drosophila provides an excellent system for addressing this issue, as there is abundant interspecific mating system variation. For example, compared to D. melanogaster subgroup species, repleta group species have higher remating rates, delayed sexual maturity, and several other interesting differences. We previously showed that accessory gland protein genes (Acp's) of Drosophila mojavensis and D. arizonae evolve more rapidly than Acp's in the D. melanogaster subgroup and that adaptive Acp protein evolution is likely more common in D. mojavensis/D. arizonae than in D. melanogaster/D. simulans. These findings are consistent with the idea that greater postcopulatory selection results in more adaptive evolution of seminal fluid proteins in the repleta group flies. Here we report another interesting evolutionary difference between the repleta group and the D. melanogaster subgroup Acp's. Acp gene duplications are present in D. melanogaster, but their high sequence divergence indicates that the fixation rate of duplicated Acp's has been low in this lineage. Here we report that D. mojavensis and D. arizonae genomes contain several very young duplicated Acp's and that these Acp's have experienced very rapid, adaptive protein divergence. We propose that rapid remating of female desert Drosophila generates selection for continuous diversification of the male Acp complement to improve male fertilization potential. Thus, mating system variation may be associated with adaptive protein divergence as well as with duplication of Acp's in Drosophila.     

Evolutionary conservation of the chromosomal configuration and regulation of amylase genes among eight species of the Drosophila melanogaster species subgroup

Nuclear DNA was extracted from each of the eight species comprising the Drosophila melanogaster species subgroup. Southern hybridization of this DNA by using a molecular probe specific for the alpha-amylase coding region showed that the duplicated structure of the amylase locus, first found in D. melanogaster, is conserved among all species of the melanogaster subgroup. Evidence is also presented for the concerted evolution of the duplicated genes within each species. In addition, it is shown that the glucose repression of amylase gene expression, which has been extensively studied in D. melanogaster, is not confined to this species but occurs in all eight members of the species subgroup. Thus, both the duplicated gene structure and the glucose repression of Drosophila amylase gene activity are stable over extended periods of evolutionary time.