Global patterns of sequence evolution in Drosophila
© Gallach et al; licensee BioMed Central Ltd. 2007
Received: 14 June 2007
Accepted: 09 November 2007
Published: 09 November 2007
Sequencing of the genomes of several Drosophila allows for the first precise analyses of how global sequence patterns change among multiple, closely related animal species. A basic question is whether there are characteristic features that differentiate chromosomes within a species or between different species.
We explored the euchromatin of the chromosomes of seven Drosophila species to establish their global patterns of DNA sequence diversity. Between species, differences in the types and amounts of simple sequence repeats were found. Within each species, the autosomes have almost identical oligonucleotide profiles. However, X chromosomes and autosomes have, in all species, a qualitatively different composition. The X chromosomes are less complex than the autosomes, containing both a higher amount of simple DNA sequences and, in several cases, chromosome-specific repetitive sequences. Moreover, we show that the right arm of the X chromosome of Drosophila pseudoobscura, which evolved from an autosome 10 – 18 millions of years ago, has a composition which is identical to that of the original, left arm of the X chromosome.
The consistent differences among species, differences among X chromosomes and autosomes and the convergent evolution of X and neo-X chromosomes demonstrate that strong forces are acting on drosophilid genomes to generate peculiar chromosomal landscapes. We discuss the relationships of the patterns observed with differential recombination and mutation rates and with the process of dosage compensation.
Drosophila melanogaster has been one of the most important animal models since the beginning of modern genetics. It was therefore obvious that its genome should be one of the first to be sequenced. Genome projects of eleven other Drosophila species are now almost finished and this provides the first opportunity to establish the global patterns of short-term genome evolution, at both the genic and chromosomal levels, in metazoans. These data are contributing to a detailed view of gene evolution, intron length evolution, selective constraints acting on non-coding sequences and many other processes [1–6].
A classical problem in molecular genetics and evolution is the characterization of the complex relationships that exist between coding sequences and repetitive elements. Changes in the repetitive component of a genome may influence all kinds of significant phenomena, from gene expression to genome size. Studies comparing Drosophila species were among the first that demonstrated that both the satellites and the middle repetitive component, mostly mobile elements, of closely related species may be very different (summarized in ). The available genomic information for drosophilids may now contribute to obtain a much more detailed picture of the impact of repetitive sequences on genome and species evolution. One of the most interesting aspects to explore is the effect that changes in repetitive DNA content may have on chromosome structure and function. Until recently, this type of study was based on conventional cytogenetic analyses plus in situ hybridization with repetitive probes. The presence in drosophilids of high-quality polytene chromosomes allowed to obtain some of the most significant results of the pre-genomic era. These included the localization of mobile elements and the determination of their rates of transposition (reviewed in ), the localization of satellite sequences, including some specifically dispersed along the euchromatin of the X chromosome [9, 10] or the demonstration that several simple DNA repeats were preferentially concentrated on the euchromatin of some chromosomes [11–13]. Particularly, Lowenhaupt et al.  used in situ hybridization with mono- and dinucleotides to obtain four main conclusions. First, they found that Drosophila subgenus species had consistently more repeats than species of the Sophophora subgenus. Later, this difference between subgenera was indirectly confirmed [14–17]. Second, they detected that three types of simple DNA repeats (CA/TG, CT/AG and C/G) were more abundant on the X chromosomes than on the autosomes of all the examined species, a result also later confirmed using different approaches [18–20]. Their third conclusion was that a chromosomal arm in D. pseudoobscura and D. miranda, which was involved in a translocation with the X chromosome and thus became a second X chromosomal arm (named XR), was also enriched for these repeats. Finally, they found that the X2 chromosome of D. miranda – originally an autosome but that now segregates as a second X chromosome because its homolog, called neo-Y, is attached in this species to the Y chromosome – contained also some regions with repeat enrichment. In Drosophila, and due to the fact that the Y chromosome lacks most of the genes present on the X, the single X chromosome of males is hypertranscribed to generate roughly the same amount of products that the two X chromosomes of the females, a process known as dosage compensation (reviewed in [21, 22]). The fact that the homolog of the XR arm of D. pseudoobscura and D. miranda degenerated and disappeared, created a similar need for XR to be dosage compensated. Finally, the neo-Y in D. miranda is partially degenerated and, therefore, the X2 chromosome is also in part dosage compensated. All these phenomena occur by the action of a dosage compensation complex (or compensasome), which recognizes and binds all the chromosomes of drosophilids that require to be compensated . The enrichment of repeats found in the works indicated above [11–13], perfectly correlated with the need for dosage compensation.
In this study, we use the information currently available for multiple Drosophila genomes to pursue the research initiated twenty years ago. We were interested in three questions. First, are there species-specific patterns of simple DNA repeats in drosophilids?. Second, is the X chromosome of drosophilids characterized by particular sequence patterns, different from those found in the autosomes?. Third, if indeed the X chromosome has peculiar patterns, which are the forces that generate them?. Here, we show that the characterization in an evolutionary context of oligonucleotide profiles (counts of overlapping words of a given size) offers insights on the forces that shape the sequences of whole chromosomes. Particularly, by comparing oligonucleotide profiles of several drosophilid species, we have obtained a precise view of how chromosomes diversify in the Drosophila genus.
X chromosome and autosomes of D. melanogaster have different compositions
General information of the sequences analyzed in this study.
Data repository and release
Muller element A
Muller element B
Muller element C
Muller element D
Muller element E
NCBI, release 3.1
UCSC genome browser, April 2005
UCSC genome browser, November 2005
UCSC genome browser, August 2005
UCSC genome browser, November 2004, freeze 2
UCSC genome browser, August 2005
UCSC genome browser, August 2005
X and autosomes show also differences in other Drosophila species
Percentage of euchromatin that corresponds to the most common mono-, di- and trinucleotides in the X chromosomes and an autosome for the seven Drosophila species.
D. mel X
D. mel 2L
D. sim X
D. sim 2L
D. yak X
D. yak 2L
D. ana X
D. ana 3R
D. pse XL
D. pse XR
D. pse 4
D. vir X
D. vir 4
D. gri X
D. gri 3
Figures 6A and 6B confirm the intraspecific results for D. melanogaster obtained above: the X chromosome has more repeats than the autosomes while two autosomes are almost identical. Moreover, the correlation coefficient values close to +1 indicate that the same sequences are present in both X chromosomes and autosomes. Figures 6C and 6D compare homologous chromosomes of two closely related species, D. melanogaster and D. simulans. It is obvious that D. melanogaster chromosomes have more repeated sequences than D. simulans chromosomes, in agreement with previous results (summarized in ; see also our Table 2 and Additional file 1). Interestingly, comparisons of Figures 6A, 6C and 6D shows that the differentiation between the chromosomes of D. melanogaster and D. simulans is quite similar to the differentiation between the X chromosome and the autosomes of D. melanogaster. This result means that a substantial degree of differentiation among chromosomes can be generated in a relatively short time, because these two species have diverged for only about 5 millions of years . Moreover, the r ≈ 1 values in the analyses shown in Figures 6C and 6D indicate that the words detected are still essentially identical in the chromosomes of these two species. Finally, in Figures 6E and 6F, homologous chromosomes of D. melanogaster and D. virilis, two species whose lineages split about 63 millions of years ago , are compared. Two results are noteworthy. First, D. virilis has much more repeated sequences than D. melanogaster in both their X chromosome and autosome. Second, composition of the chromosomes is, for these two species, somewhat different. The r values are quite smaller than those obtained intraspecifically. These results thus globally confirm the differences described in Table 2.
X/X ratio values among Drosophila species (k = 13).
D. mel. X
D. sim. X
D. yak. X
D. ana. X.
D. pse. XL
D. vir. X
D. gri. X
D. mel. X
D. sim. X
D. yak. X
D. ana. X
D. pse. XL
D. vir. X
D. gri. X
Evolution of the neo-X chromosomal arm of D. pseudoobscura
We have shown that the X chromosomes and the autosomes of Drosophila species have different global compositions. The X chromosome is enriched in simple repeats and also contains, in some species, complex X chromosome-specific sequences. On the other hand, all autosomes within a Drosophila species have identical compositions. There is however variation among species, with those in the melanogaster group being the ones with the highest level of global X chromosome specificity and D. pseudoobscura the one with the lowest (Figure 4). The enrichment of simple DNA sequences on the X chromosome is not accompanied by a general modification of the types of repeats. In all species tested, the words found on the X and on the autosomes are the same, only their frequencies change. This is shown by the high correlations observed for comparisons between X and autosomes (Figures 6, 8). A significant difference in chromosome composition is detected for comparisons between Drosophila subgenus and Sophophora subgenus species. Sophophorans contain less simple repeated DNA (Tables 2, 3; Additional file 1). This result correlate with the fact that the two species of the Drosophila subgenus have larger euchromatic genomes (about 140 Mb) than the rest (about 120 Mb; data from  at the DroSpeGe web page. See ). In fact, simple DNA repeats could explain a substantial part of the differences in genome size. The repeats detailed in Table 2 (a fraction of the total present in those chromosomes) account for about 6 Mb of the 117 Mb euchromatic genome of D. simulans and for about 12 Mb of the 140 Mb euchromatic genome of D. grimshawi. This means that they alone explain about 26% (6/23) of the difference of euchromatic genome size between these two species. Even after all these results, before concluding that this difference between subgenera is general we must consider that the number of species examined is still small. In fact, indirect results suggest that some species may not fit this pattern. For example D. subobscura, a sophophoran species quite closely related to D. pseudoobscura, seems to have many repeats . In addition, there is evidence for significant differences among closely related species of the Drosophila subgenus .
The finding that D. melanogaster has many (AC/TG)n, (AT/AT)n,(AG/CT)n and (A/T)n repeats was previously described by other authors [13, 18, 32, 33]. We have detected also a considerable proportion of (AAC/GTT)n, (AGC/GCT)n and (AAT/ATT)n simple sequences in this species. These are also the predominant repeats in the rest of melanogaster group species. In addition, all the species of this group have considerable amounts of X chromosome-specific satellites, which are especially frequent in D. ananassae (see Additional file 1). In general, the most abundant simple repeats in melanogaster group species are also the most abundant in the rest of drosophilids. However, there are some differences. For example, melanogaster group species contain less (AG/CT)n repeats than the rest (Table 2). These subtle differences, together in some cases with the appearance of species-specific sequences (D. virilis, D. ananassae), lead to global changes when homologous chromosomes of distantly related species are compared (e. g. Figure 6; D. melanogaster – D. virilis comparisons). Modifications of the sequences of these chromosomes occur at a relatively rapid timescale (see also Figure 6; D. melanogaster – D. simulans comparisons). A final significant result is that we have observed convergence in the global sequence pattern between the XL and XR arms of D. pseudoobscura. The conversion of XR from an autosome into a neo-X chromosomal arm has led to an increment in its amount of simple DNA repeats up to levels which are identical to those in XL, the original arm of the X chromosome (Figures 7 and 8). This process, occurred in the last 10 to 18 millions of years, suggests that the X chromosome in a given species has an optimal composition, different from the autosomes, to which neo-X chromosomes tend.
We may now ask which are the forces that are behind all these patterns. In our opinion, the systematic finding of X-chromosome specificity in all species, the almost identical results for autosomes within a species, the correlation between evolutionary relatedness and differences in the simple DNA components and the finding of convergence between the XL and XR chromosomal arms rule out that these changes are due to chance alone. Systematic forces must be operating that contribute to X chromosome differentiation from the autosomes and to autosome homogeneity within a species. Related forces must explain why different species have different amounts and types of simple DNA repeats. Understanding the causes of these patterns may be of broad interest, because similar trends are present in other animal species. For example, results in primates are consistent with a rapid modification of repeat content in closely related species and differences in simple repeats between the X chromosome and the autosomes have been also observed [34–37].
A first interesting question is how to explain differences between closely related species such as the ones that we have studied. This is a classical problem. Several authors have recently discussed the reasons why related organisms have different amounts of non-coding and/or repetitive DNA, often in the context of the impact that those changes may cause on genome size [38–45]. The summary is that there are many forces that influence the global composition of genomes. Some of them imply differences in mutation rates while others are related to changes in selective regimes. The problem is that the particular contributions of those forces are unknown. For example, genome size tends to correlate with increases in simple DNA and microsatellites [40, 42, 46], increases in intron size (e. g. ref. ), increases in transposable element number , etc, while a high rate of nucleotide deletion tends to correlate also with a small genome size [48–50]. However, none of these forces fully determines genome size, which leads to multilevel hypotheses involving many different parameters (see discussions in [38, 43, 44, 51]).
We can rule out some possible explanations for the observed interspecific differences in the amounts of simple DNA sequences. For example, changes do not seem to correlate with external features, such as the geographical distribution of these species, which might be associated to differences in life history traits. D. simulans and D. virilis, which are in the extremes of the distribution of simple DNA content, are both human commensals and thus widely distributed . Also, a weak correlate can be obtained between size of the organisms and simple DNA content (and genome size), because D. virilis and, especially, D. grimshawi individuals are bigger than the sophophoran species considered. However, organism size obviously does not explain the differences observed for D. melanogaster and D. simulans, two sibling species.
Agreement with internalist hypotheses is also difficult. Some simple explanations can be probably dismissed. For example, the rate of DNA deletion does not correlates well with simple DNA content, because D. melanogaster and D. virilis have similar rates . The rate of point mutations in unconstrained regions seems to be also similar in D. virilis and melanogaster group species . It is unclear whether recombination contributes to explain the patterns observed. On one hand, increased recombination may decrease genome complexity if recombination favors the generation of repeats. On the other hand, selective pressure to increase simple DNA repeats, for them to act as recombinogenic sequences, could occur in some species (see Refs. [42, 54–58]). In either case, we would expect a strong correlation between recombination rates and amounts of simple DNA repeats. However, in drosophilids, this correlation is not obvious. First, we would expect a decrease in simple DNA repeats in species with low chromosomal polymorphism, which lack inversions that restrict recombination. However, this pattern is not observed. For example, D. simulans is chromosomically monomorphic (reviewed in ), but so is D. virilis . In addition, the length of the chromosomes in map units, an indication of the likelihood of recombination, correlates only partially with the amount of simple repeats. For example, in reasonable agreement with their respective amounts of simple DNA repeats, the X chromosome of D. virilis has 170.5 map units, while the D. pseudoobscura XL chromosome has 157.6 units and the D. simulans X chromosome only about 66 [61–63]. However, D. simulans has total map distances which are about 30% longer than those of D. melanogaster , while the amount of repeats in all D. simulans chromosomes is smaller. In particular, the X chromosome has about the same length in recombination units in those two species , in spite of their significant difference in repetitive DNA (Figure 6C). In summary, although differential recombination rates may contribute to generate the patterns observed, they cannot explain them all.
Apart from recombination, there are three internal forces able to increase repeatedness that may also contribute to explain the interspecific differences obtained. First, differential intrinsic slippage rates among species, generating more abundant and larger microsatellites in some of them. Second, species-specific amplification of satellites. Third, an increase in mobile element number in some species. These three forces may positively correlate. We have obtained evidence for a relevant decrease in chromosome complexity in some species to be associated to the amplification of relatively complex, repeated sequences (X-linked satellite in melanogaster group species; complex repeated sequences in D. ananassae and D. virilis). In the case of the 36 bp sequence detected in D. virilis, it has been described as included in a putative mobile element called pDv . It has been suggested that differential amplification of mobile elements may change in a short time the global sequence pattern of a chromosome, especially if the elements have simple internal sequences that contribute to the generation of new microsatellites . So far, evidence for this type of process is not strong, but we have not found any result contradicting this hypothesis, so it deserves further study.
A second pattern that requires explanation is why X and autosomes are so different. This could be due to either mutational or selective forces acting differentially in X chromosomes vs. autosomes. In Drosophila, at least in analyses involving closely related species, there is no evidence for strong differences in mutation or selective regimes acting on coding regions of the X chromosome versus those found in the autosomes (reviewed in ). In our opinion, this leaves open two possible explanations. The first option is differential recombination rates among chromosomes. Due to the fact that in Drosophila males do not recombine, two thirds of the X chromosomes but only two fourths of the autosomes recombine in each generation. Given a positive association between recombination and generation of repeats, this could lead to an increase of repeats on the X chromosomes. We think however that recombination may again contribute but does not fully explains our results. This hypothesis predicts a correlation between relative recombination rates and relative amounts of repeats that it is not observed. Thus, comparing D. melanogaster, a species with a high X/A ratio, with D. pseudoobscura, the species with the lowest X/A ratio (Table 2), we would expect the former to have higher relative recombination rates in the X respect to the autosomes. However, the opposite if found. For example, the X/2L relative euchromatic recombination rate is 1.22 for D. melanogaster (data from Flybase.org) while the same rate for the homologous chromosomes of D. pseudoobscura (X/4) is 1.94 . Thus, recombination may influence but does not seem to determine the relative proportion of repeats in X chromosomes and autosomes.
The second posible explanation is that the pattern observed derives from a functional requirement for simple repeats on the X. Our favorite explanation is that it is related to the need of dosage compensate the X chromosome. More precisely, the acquisition of dosage compensation might require a modification of the DNA of a chromosome to make it more repetitious. This could be caused by the dosage compensation complex using simple sequences to recognize the X chromosome. Alternatively, an increase in simple DNA might contribute to increased transcriptional levels by allowing the complex to act on appropriate chromatin domains (see discussion in ). The idea that repeats in some way contribute to dosage compensation is old, but always lacked empirical support (e. g. see comment in ). Several recent analyses of the dosage compensation complex binding sites do not really confirm or refute this hypothesis, because no obvious consensus sequence required for binding has emerged [67–71]. However, results obtained by Peter Becker's group [68, 69, 71] suggest that repetitious sequences, rich in CA/TG and GA/TC dinucleotides, may cooperate to facilitate the binding of the complex. If this is the case, X chromosome-specific binding could be achieved by increasing the density of simple DNA repeats on the X respect to the autosomes. Interestingly, a related situation seems to explain the recognition of the X chromosome by the Caenorhabditis elegans dosage compensation complex [72, 73]. Dosage compensation in humans, associated to X chromosome inactivation, may also be related to the enrichment of repetitive sequences on regions of the X chromosome [74–76].
As a final aside, we must point out that this work shows how useful is to perform oligonucleotide profiling studies of eukaryotic chromosomes using long words (e. g. k = 13). The subtle differences that exist among chromosomes or among species can be very simply uncovered by analyses using long, rare, words, while they are difficult to demonstrate when shorter, more unspecific sequences are analyzed. For example, Stenberg et al.  characterized by multivariate analyses the differences between chromosomes of D. melanogaster, D. simulans and D. pseudoobscura, using short words (up to k = 6). With hexamers, they found strong characteristic signatures of the Muller F elements (dot chromosomes) of these species and just a weak differentiation of the X chromosomes of D. melanogaster and D. simulans, but not D. pseudoobscura, respect to their autosomes. With our approach, based on larger words, we have detected clear differences for all three species.
Oligonucleotide profiling allows for a rapid characterization of the patterns of sequence evolution. We have shown that chromosome profiles are quite similar among Drosophila species, with the X chromosome being always simpler than the autosomes. However, the particular sequences that confer this simplicity to the X vary among species. The differences observed among closely related species and the identical profiles of X and neo-X chromosomes suggest that strong forces are acting on relatively short periods of time to generate these patterns. We suggest that the combined effects of differential recombination, differential generation of simple DNA repeats and natural selection caused by the need of dosage compensation may explain our results.
We used genomic data for five species of the Sophophora subgenus and two species of the Drosophila subgenus. Within the Sophophora subgenus, four species of the melanogaster group (D. melanogaster, D. simulans, D. yakuba and D. ananassae) and one species from the obscura group (D. pseudoobscura) were analyzed. The two Drosophila subgenus species were D. virilis (virilis group) and D. grimshawi (hawaiian Drosophila). These species were chosen for two reasons. First, to cover all the range of divergence times within the genus, from perhaps 5 millions of years of divergence (D. melanogaster – D. simulans) to about 63 millions of years (species of the Sophophora subgenus vs. species of the Drosophila subgenus) . Second, because at the time we started our study (beginning 2006) they were, among the eleven ongoing drosophilid genome projects, the ones with the best available sequences. Table 1 describes the sequences used in this study – ordered according to the standard nomenclature of Muller elements, which correspond to homologous chromosomal arms – and their origin. We centered our attention on the X chromosomes and the longest autosomes. The dot chromosomes (Muller F elements) were not considered. All the analyzed sequences were euchromatic. For D. melanogaster, D. simulans and D. yakuba, the chromosomes were already assembled in the databases. For D. pseudoobscura, we added together all the pieces of a same chromosome in a single file. Finally, for the other three species we added together several scaffolds that corresponded to regions homologous to D. melanogaster chromosomes. Sizes of the final files ranged from 10.7 to 29.7 megabases (Mb). According to the most recent data (December 2006 assembly of the Drosophila genomes; see  and the DroSpeGe database ), these files contained from about 71.1% (D. grimshawi) to 97.2% (D. pseudoobscura) of the euchromatin of these species, with the average being 85.2%. Therefore, an assuming no extreme biases occurred in the sequencing projects, our samples may be considered fully representative of their euchromatic genomes.
Characterization of the chromosomal profiles was performed using a program called UVWORD . This program characterizes, using a sliding-window approach, all overlapping oligonucleotides of a particular size k present in a particular sequence (target sequence) and then establishes their frequency in another sequence (source sequence). The user may select a value of k such that 1 ≤ k ≤ 14. If source and target sequences are the same, for example a particular chromosome, the program provides the frequency of all oligonucleotides of the chosen size k in that chromosome. If, on the other hand, source and target are two different chromosomes, the program counts how many times each oligonucleotide in the target chromosome is present in the source chromosome. Comparison of the results for two different sources allows for a rapid characterization of the similarity of two DNA sequences (see below: Chromosomal comparisons; ). Along this work, we have used values of k ranging from 1 to 13 nucleotides. Most of the analyses requiring long words were performed using 13 nucleotides. In general, we preferred k = 13 because 13 is a prime number, being thus less affected by the presence of repeats based on dinucleotides, trinucleotides, etc. In all analyses, results for both chains of the DNA molecules were added together. Complex repeats in D. ananassae and D. virilis were manually assembled from results in Additional file 1.
Calculation of the number of sites containing simple DNA sequences
Because UVWORD counts overlapping words, a microsatellite may generate adjacent identical sequences that will be counted multiple times (e. g. with k = 13, a (CA)8 microsatellite will generate two CACACACACACAC and two ACACACACACACA sequences). Therefore, this program cannot count the number of independent sites in which a particular perfect repeat is present along a chromosome. To solve this problem, we generated a second program, called UVCOUNT. This program searches for a given sequence or arbitrary size establishing its frequency and positions in a DNA sequence. After UVCOUNT analyses were completed, results were filtered, in order to count just once the words that overlap. This combined analyses provided the number of independent loci that contained a sequence of interest and their positions. Only strings of six or more nucleotides (i. e. at least six contiguous identical mononucleotides, three contiguous identical dinucleotides or two identical trinucleotides) have been counted in the analyses shown in Table 2. In those analyses, again, results for both chains of a double helix were counted together.
To obtain a global value of similarity for two chromosomes, we first obtained the counts for all oligonucleotides present in the target sequence (one of the two chromosomes) in each of the two source sequences (i. e. each of the two chromosomes in which we were interested, which we called "source 1" and "source 2" above). For each chromosome, the counts were summed and averages were obtained. Then, the averages of both sources were divided one by the other. This final proportion was corrected to account for differences in size between the two sequences. In random sequences of long size, this final corrected value would be about 1.
This work was supported by Grant SAF2006-08977 (Ministerio de Educación y Ciencia, Spain).
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