MBE Advance Access originally published online on September 8, 2005
Molecular Biology and Evolution 2006 23(1):162-167; doi:10.1093/molbev/msj012
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
Differences in Genome Size Between Closely Related Species: The Drosophila melanogaster Species Subgroup
* Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, CNRS, Université Claude Bernard Lyon 1, Villeurbanne Cedex, France and Centre de Génétique Moléculaire et Cellulaire, UMR 5534 CNRS, Université Claude Bernard Lyon 1, Villeurbanne Cedex, France
E-mail: biemont{at}biomserv.univ-lyon1.fr.
 |
Abstract |
|---|
 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
Genome size varies considerably among organisms due to differences in the amplification, deletion, and divergence of various kinds of repetitive sequences, including the transposable elements, which constitute a large fraction of the genome. However, while the changes in genome size observed at a wide taxonomic level have been thoroughly investigated, we still know little about the process involved in closely related species. We estimated genome sizes and the reverse transcriptase–related sequence (RTRS) content in the nine species of the Drosophila melanogaster species subgroup. We showed that the species differ with regard to their genome size and that the RTRS content is correlated with genome size for all species except Drosophila orena. The genome of D. orena, which is 1.6-fold as big as that of D. melanogaster, has in fact not undergone any major increase in its RTRS content.
Key Words: Drosophila • genome size • phylogeny • transposable elements • satellite DNA
|
Introduction |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
The wide variation in haploid genome size, more than 200,000-fold between different eukaryotes (Gregory 2005
), results mainly from differences in the amounts of various kinds of repetitive sequences including transposable elements (TEs) (Kidwell 2002), which constitute a large fraction of the genome (Keyl 1965; Flavell 1980; Black and Rai 1988; Warren and Crampton 1991; Pagel and Johnstone 1992; SanMiguel et al. 1996; Uozu et al. 1997; Gregory and Hebert 1999; Petrov 2001). These differences in the TE amount could be interpreted as differential amplification of TEs between lineages. One striking example comes from maize, the genome of which has doubled in size over a few million years as a result of a burst of retrotransposon transposition (SanMiguel et al. 1996). This has led to the idea that genomes can only increase in size (Bennetzen and Kellogg 1997). However, it has now been clearly established that genome expansion via the amplification of various repeated sequences is reversible as a result of illegitimate recombinations (Devos, Brown, and Bennetzen 2002) or intraelement LTR (Long Terminal Repeat)-LTR recombination (Shirasu et al. 2000; Ma and Bennetzen 2004), although this mechanism can only slow genomic growth by retrotransposons. Moreover, it seems that in mammals and insects small deletions occur more often and tend to be larger than small insertions (the indel bias, see Petrov, Lozovskaya, and Hartl 1996; Bensasson et al. 2001). DNA loss due to deletion within the TE sequences (Lozovskaya et al. 1999) thus provides an additional mechanism by which genome size can decrease, although some authors have raised doubts about the importance of this phenomenon with regard to changes in genome size (Charlesworth 1996; Gregory 2004). Differing rates of amplification and deletion are, therefore, assumed to have contributed to the very different DNA contents observed in related organisms (Lozovskaya et al. 1999; Singh and Petrov 2004). Although phylogenetic approaches suggest that increases and decreases of DNA contents have occurred repeatedly during evolution (Wendel et al. 2002; Ma, Devos, and Bennetzen 2004) and have involved operating forces that differ across different genomic regions and components (Grover et al. 2004), most of these studies have looked at large taxonomic groups.
Interspecies differences in genome size have long been contrasted to the constancy of DNA content within a given species. However, intraspecific variations have also been reported and have sometimes been related to environmental conditions, suggesting that genome size is a selective trait associated with cell and body size (Gregory 2001) and/or that TEs may be mobilized in response to stressful environmental conditions (Brezinsky, Humphreys, and Hunt 1992; Arnault and Dufournel 1994; McDonald 1995; Vieira et al. 1999; Hagan, Sheffield, and Rudin 2003). Such intraspecific differentiation has been associated with differences in the amount of chromosomal heterochromatin in different populations (Sherwood and Patton 1982), suggesting that quick and drastic processes exist that are able to reshape genomes within a few generations. This implies that variations in genome size might be detectable between very closely related organisms. In order to investigate the evolution of genome size at this scale, we compared genome size of the nine species of the Drosophila melanogaster subgroup, which diverged from their most recent common ancestor 10–15 MYA (Li, Satta, and Takahata 1999; Lachaise and Silvain 2004). Genome size was estimated by flow cytometry, and the amount of reverse transcriptase–related sequences (RTRS) was determined by dot blots. We showed that the species from this group differ with regard to their genome size and that the RTRS content is correlated with genome size for all species except Drosophila orena. The genome of D. orena, which is 1.6-fold as big as that of D. melanogaster and is known to harbor a high amount of satellite DNA (Barnes, Webb, and Dover 1978; Strachan et al. 1982), has in fact not undergone any major increase in its RTRS content.
|
Materials and Methods |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
The Drosophila Group
The D. melanogaster species subgroup is composed of nine species of Afro-tropical origin. Drosophila melanogaster and Drosophila simulans are cosmopolitan species; Drosophila sechellia and Drosophila mauritiana are endemic to the Seychelles and Mauritius Islands and are closely related to D. simulans, constituting the simulans clade; Drosophila erecta and D. orena are restricted to west central Africa; Drosophila yakuba and Drosophila teissieri are localized in an area spreading from northwest to southeast Africa, while Drosophila santomea, a close relative of D. yakuba, seems to be limited to the Sao Tome Island in the Gulf of Guinea, where it was discovered recently (Lachaise et al. 2000
). The three species D. yakuba, D. santomea, and D. teissieri and the two species D. erecta and D. orena constitute two distinct clades within the D. melanogaster species subgroup (see phylogeny in fig. 1). We studied 16 and 17 populations from different geographical origins for D. melanogaster and D. simulans, respectively, and one stock for each of the other species.
|
Estimation of the Genome Size
The genome size was estimated by flow cytometry using nuclei from the heads of adult flies (Vieira et al. 2002
; Nardon et al. 2003, 2005). Measurements were done in two independent experiments. The estimated genome size was expressed as the relative fluorescence intensity (the ratio of the fly fluorescence intensity to the Tetraodon nigroviridis fluorescence intensity used as the internal control) rather than the absolute genome size of the fly nuclei (Nardon et al. 2003). The absolute genome sizes of the flies can be obtained by multiplying the relative intensity values by the size of the T. nigroviridis haploid genome, which is usually taken to be 0.5 pg. Because genome size estimates obtained by flow cytometry vary according to physiological state of the individuals and environmental conditions (Nardon et al. 2003), we preferred to calculate only the relative intensity, which does not depend on the genome size assumed for the tetraodon (see Jaillon et al. 2004).
Dot Blot Experiments
To investigate the mechanisms responsible for the variations of genome size in the D. melanogaster species subgroup, we estimated the proportion of retrotransposons (the RNA-based elements) in the genomes by analyzing the global amount of RTRS. Although this approach did not give a complete picture of all kinds of TE families, it did reveal some of the most common families in the Drosophila genome (Lerat, Rizzon, and Biémont 2003; Rizzon et al. 2003).
Genomic DNA from the different species was blotted on a nylon membrane that was hybridized with a degenerate oligonucleotide (hereafter referred to as the Reverse Transcriptase [RT]-oligonucleotide) corresponding to the YXDD box, which is highly conserved among reverse transcriptases (Warren and Crampton 1991). This gave a signal proportional to the amount of RTRS in the different spots. Because the RT-oligonucleotide was very short and degenerate, part of the signal obtained was attributable to nonspecific hybridization. This tended to homogenize the signal between spots, and so the differences found in the proportion of RTRS between the species were likely underestimated.
The membrane was then dehybridized and probed again with the single-copy gene RP49 cloned from Drosophila pseudoobscura. We used the sequence from D. pseudoobscura because this species diverged from the D. melanogaster subgroup around 25–55 MYA (Tamura, Subramanian, and Kumar 2004), and the sequence of its RP49 gene must have diverged to the same level on average from the species of the D. melanogaster subgroup. Assuming that the RP49 gene has evolved at the same rate in the different lineages of the D. melanogaster subgroup phylogeny, the signal's intensity was expected to be proportional to the amount of DNA spotted on the membrane. The amount of RTRS per single-copy gene (hereafter referred to as the RT-oligonucleotide/RP49 ratio) was thus estimated by dividing the intensity obtained with the RT-oligonucleotide by the signal obtained with the RP49 gene. These experiments were repeated for two different membranes. Because of space limitation on the membranes, only two populations of D. melanogaster and D. simulans were used for the dot blot experiments.
Total genomic DNA was extracted from 40 males of each species by a standard phenol-chloroform method after proteinase K digestion. For each species, five quantities of DNA (4, 1, 0.25, 0.0625, and 0.0156 µg) were spotted on a nylon Hybond-N+ membrane (Amersham, Orsay, France). The membrane was prehybridized overnight at 30°C in 6 x saline sodium citrate (SSC), 0.6% sodium dodecyl sulfate (SDS), 5 x Denhardt's solution, and denatured herring sperm DNA (100 µg/ml) and hybridized for 18 h with the RT-oligonucleotide (5'-TAYGTNGAYGAYATG-3') probe. The membrane was then washed once for 5 min in 6 x SSC, 0.1% SDS, and twice for 5-min periods in 4 x SSC, 0.1% SDS at 22°C. The radioactivity bound to the membrane was measured using a molecular imager (Model GS-525, BioRad, Marnes-la-Coquette, France). The RT-oligonucleotide probe was then removed by washing the membrane twice in 0.4 N NaOH. A measurement with the molecular imager was performed to check that the probe had been uniformly removed. The membrane was then prehybridized overnight at 42°C in 50% formamide, 5 x SSC, 0.5% SDS, 5 x Denhardt's solution, denatured herring sperm DNA (100 µg/ml), and hybridized for 18 h with the RP49 probe. The membrane was then washed once in 5 x SSC, 0.5% SDS, and twice in 1 x SSC, 0.1% SDS at 42°C. The radioactivity was measured as indicated above.
The RT-oligonucleotide was 5' labeled with 32PdATP using a polynucleotide kinase (NEB), and the RP49 probe was labeled with 32PdCTP using a random priming kit from Amersham. RP49 was amplified from D. pseudoobscura with primers 5'-AAGATCATCAAGAAGCGCAC-3' and 5'-ACTCGTTCTCTTGAGAACGC-3' then cloned using the TOPO TA Cloning kit (Invitrogen, Cergy Pontoise, France).
|
Results |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
Figure 1 shows the estimated genome sizes of the nine D. melanogaster subgroup species represented according to their phylogeny (Lachaise and Silvain 2004
), plus D. pseudoobscura, considered as the outgroup. As the second estimate was always greater than the first estimate, the values should be compared within each experiment but not between them. However, the ranking of the genome sizes were very similar for both experiments (Spearman's rank correlation coefficient 
= 0.95, P < 0.001). Drosophila orena genome size estimates appear to be about 1.6-fold greater than the next biggest genome size estimate in both experiments. The differences between the genome size values were less pronounced for the other species, although the variations in genome size among these species are significant. Indeed a two-way analysis of variance detected the effects of the experiment (F = 30.8, P < 0.001) and that of the species (F = 119.4, P < 0.001). Among these species, two groups can be distinguished with regard to genome size: a first group, with a genome size ratio between 0.45 and 0.47 for the first estimate and between 0.46 and 0.48 for the second estimate, includes D. melanogaster, D. sechellia, D. yakuba, and D. santomea; a second group, with a genome size ratio ranging from 0.40 to 0.42 for the first estimate and from 0.41 to 0.43 for the second estimate, includes D. simulans, D. mauritiana, D. erecta, and D. teissieiri. The estimate for D. pseudoobscura lies within the second group. The low variability in genome size values observed among the 16 population samples of D. melanogaster and among the 17 population samples of D. simulans (fig. 2) suggests that the flow cytometry technique worked very reliably and indicates that the estimated genome size of the different species can be viewed as being highly trustworthy, even though some species were characterized by only one population sample.
|
Figure 3 shows the relationship between genome sizes expressed as the mean of the values from the two experiments and the RT-oligonucleotide/RP49 ratios for the two membranes analyzed. As the RT-oligonucleotide/RP49 ratio depends on several factors (the probe-specific activity, the duration of exposure, etc), the absolute values of the ratio should not be compared between the different membranes. However, the ranking of the ratio values were very similar in both membranes (Spearman's rank correlation coefficient
= 0.85, P < 0.01, see fig. 3), suggesting that the data were very consistent. The position of D. orena in this diagram is striking, as its dot blot ratio value lies within the range of values found for the other species, which contrasts to what was expected on the basis of its high estimated genome size. Excluding D. orena from the analysis leads to a statistically significant positive correlation between the dot blot ratio values of the other species and their genome size estimates (r = 0.76, P < 0.01 and r = 0.64, P < 0.05 for membranes 1 and 2, respectively). This suggests that the differences between the genome size estimates can be explained in part by differences in the proportions of RTRS amount, except for D. orena.
|
|
Discussion |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
The overall picture that emerges from the data is that genome size differs significantly between the closely related species of the melanogaster subgroup and that part of this variation is attributable to differences in the amount of RTRS. Three groups of species can be distinguished on the basis of their estimated genome sizes: the first group consists of D. melanogaster, D. sechellia, D. yakuba, and D. santomea; the second group consists of D. simulans, D. mauritiana, D. erecta, and D. teissieiri. Drosophila orena constitutes the third group, with an estimated genome size about 1.6-fold that of the other species. This grouping by genome size differs from the phylogenetic grouping, suggesting that parallel but independent changes in genome size have occurred in the different lineages. What scenario based on increases and/or decreases in genome size over time is most likely to account for these differences in genome size within the phylogeny? Because it was impossible to find out whether the increase or decrease in the DNA content is the preponderant force and because some processes could act in a discontinuous way, we did not attempt to use quantitative parsimony algorithms to assess the genome size of the ancestors in the phylogeny.
Drosophila orena differs considerably from the other species in that its much greater increase in genome size cannot be attributed solely to an increase in its RTRS amount. This species is known to have an extraordinary karyotype, with a large amount of heterochromatin and hence of satellite DNA sequences (tandemly organized, highly repeated DNA sequences) (Barnes, Webb, and Dover 1978; Strachan et al. 1982). Thirty percentage of the nuclear DNA of this species is satellite DNA, and hybridization experiments have shown that the amplified satellite DNA family is species specific (Strachan et al. 1982). The change in genome size of D. orena appears, therefore, to result from the amplification of a limited number of families of satellite DNA, such as the 1668 and 180 satellites (Strachan et al. 1982), which has not been accompanied by the simultaneous amplification of RTRS.
Because D. orena seems to be a relic species, which is only known to occur in the high mountains (2,100 m altitude) of Cameroon, this raises the question as to whether its change in genome size has played a causative role in its adaptation to its peculiar environment (Knight, Molinari, and Petrov 2005) or is simply subsequent to or a consequence of speciation. If the increase in genome size has resulted from selection for a larger genome, we could expect to observe larger introns, as usually observed in animals (Moriyama, Petrov, and Hartl 1998; Vinogradov 1999). However, a study done by Parsch (2003) did not reveal any increase in D. orena introns.
Because the genome size of D. orena is exceptional compared to that of the other species, we can exclude this species from any attempt to provide a global interpretation of the differences in genome size among the species of the D. melanogaster subgroup. The present genome size of a species is the outcome of the DNA gain due to the amplification of repeated sequences and DNA loss by homologous, unequal, and illegitimate recombination (Ma and Bennetzen 2004) and the indel bias in favor of deletions. DNA gain, as the result of the amplification of repeated sequences, is well documented, especially in plants (SanMiguel et al. 1996), and may be a quick process. DNA loss, as a result of homologous recombinations, has been shown to severely reduce genome size in plants by eliminating LTR retrotransposons, and its frequency varies between species (Bennetzen, Ma, and Devos 2005). This kind of recombination, which involves the recombination of two LTRs, therefore, seems to be limited to retrotransposons, while illegitimate recombination may eliminate large stretches of DNA and can affect all kinds of repeated DNA sequences. Indel bias has been shown to be very strong in Drosophila and may explain the absence of pseudogenes in this group (Petrov, Lozovskaya, and Hartl 1996). The net result of these processes may thus be an increase in genome size compared to the ancestor, a decrease or relative apparent stability. What scenarios are likely to account for the observed genome sizes of the two groups of species?
Let us consider the species D. melanogaster and D. sechellia. These two species have similar genome sizes, which may have resulted from a decrease from an ancestor with a higher genome size or from an increase from an ancestor with a smaller genome size. However, D. melanogaster is known to have many active TEs, with numerous insertion sites along the chromosome arms as well as copies within the chromocenter (Biémont et al. 1994; Lerat, Rizzon, and Biémont 2003), whereas D. sechellia is characterized by having few TE copies on its chromosome arms, but many copies mostly embedded within the heterochromatin of its large chromocenter (Montchamp-Moreau et al. 1993; Cizeron et al. 1998). This suggests that these two genomes have been subjected to a different process of evolution and that their similar genome sizes have resulted from differing TE amplification and distribution patterns. This does not mean, of course, that DNA loss has not occurred in these species but just that D. melanogaster and D. sechellia differ from their common ancestor by independent accumulations of repeated sequences, including TEs. Drosophila yakuba and D. santomea may also have been subjected to an increase in their genome size from that of the common ancestor, but in a way that is independent of the processes in D. melanogaster and D. sechellia. Unfortunately, we do not have any information about the precise composition of the genomes of D. yakuba and D. santomea, which could indicate how this increase has happened.
If the first group of species has undergone an increase in genome size from that of their ancestor, then the second group, which has a smaller genome size, may have undergone only minor changes from the ancestor. Because D. pseudoobscura also has a small genome size, similar to that of this second group of species, it is likely that the value of the genome size of the ancestor of all the species of the Drosophila species subgroup was close to the value for the second group, which would indicate an apparent stability of genome size. Insertions and deletions certainly have occurred in these species, but in a way that has not greatly affected their genome composition. It is thus parsimonious to assume that the species D. simulans, D. mauritiana, D. erecta, D. teissieiri, and perhaps D. pseudoobscura have undergone only slight genome changes. Of course, drastic and independent changes in genome size cannot be ruled out, but this seems unlikely in the face of the very similar genome size values found in these species.
Our data show that genomes of the same size may have undergone highly different patterns of evolution and that genomes are subjected to constant change in their composition, if not in their size.
|
Acknowledgements |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
We would like to thank M. L. Cariou, D. Lachaise, and F. Lemeunier for their gift of the Drosophila subgroup species samples; A. Heddi, B. Loppin, and N. Mugnier for technical advices; C. Nardon for invaluable help; C. Vieira and J. Varaldi for their comments; and M. Ghosh for revising the English text. This work was funded by the Centre National de la Recherche Scientifique (UMR 5558, GDR 2157).
|
Footnotes |
|---|
Pierre Capy, Associate Editor
|
References |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
Arnault, C., and I. Dufournel. 1994. Genome and stresses: reactions against aggressions, behavior of transposable elements. Genetica 93:149–160.[CrossRef][ISI][Medline]
Barnes, S. R., D. A. Webb, and G. Dover. 1978. The distribution of satellite and main-band DNA components in the melanogaster species subgroup of Drosophila. I. Fractionation of DNA in actinomycin D and distamycin A density gradients. Chromosoma 67:341–363.[CrossRef][ISI][Medline]
Bennetzen, J. L., and E. A. Kellogg. 1997. Do plants have a one-way ticket to genomic obesity? Plant Cell 9:1509–1514.[CrossRef][ISI][Medline]
Bennetzen, J. L., J. Ma, and K. M. Devos. 2005. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95:127–132.
Bensasson, D., D. A. Petrov, D. X. Zhang, D. L. Hartl, and G. M. Hewitt. 2001. Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol. Biol. Evol. 18:246–253.
Biémont, C., F. Lemeunier, M. P. Garcia Guerreiro, J. F. Brookfield, C. Gautier, S. Aulard, and E. G. Pasyukova. 1994. Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster. Genet. Res. 63:197–212.[ISI][Medline]
Black, W. C. IV, and K. S. Rai. 1988. Genome evolution in mosquitoes: intraspecific and interspecific variation in repetitive DNA amounts and organization. Genet. Res. 51:185–196.[ISI][Medline]
Brezinsky, L., T. D. Humphreys, and J. A. Hunt. 1992. Evolution of the transposable element Uhu in five species of Hawaiian Drosophila. Genetica 86:21–35.[CrossRef][ISI][Medline]
Charlesworth, B. 1996. The changing sizes of genes. Nature 384:315–316.[CrossRef][Medline]
Cizeron, G., F. Lemeunier, C. Loevenbruck, A. Brehm, and C. Biémont. 1998. Distribution of the retrotransposable element 412 in Drosophila species. Mol. Biol. Evol. 15:1589–1599.[Abstract]
Devos, K. M., J. K. M. Brown, and J. L. Bennetzen. 2002. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12:1075–1079.
Flavell, R. A. 1980. The transcription of eukaryotic genes. Nature 285:356–357.[CrossRef][Medline]
Gregory, T. R. 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. Camb. Philos. Soc. 76:65–101.[Medline]
———. 2004. Insertion-deletion biases and the evolution of genome size. Gene 324:15–34.[CrossRef][ISI][Medline]
———. 2005. The C-value enigma in plants and animals: a review of parallels and an appeal for partnership. Ann. Bot. 95:133–146.
Gregory, T. R., and P. D. Hebert. 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9:317–324.
Grover, C. E., H. Kim, R. A. Wing, A. H. Paterson, and J. F. Wendel. 2004. Incongruent patterns of local and global genome size evolution in cotton. Genome Res. 14:1474–1482.
Hagan, C. R., R. F. Sheffield, and C. M. Rudin. 2003. Human Alu element retrotransposition induced by genotoxic stress. Nat. Genet. 35:219–220.[CrossRef][ISI][Medline]
Jaillon, O., J. M. Aury, F. Brunet et al. (58 co-authors). 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957.[CrossRef][Medline]
Keyl, H. G. 1965. A demonstrable local and geometric increase in the chromosomal DNA of Chironomus. Experientia 21:191–193.[CrossRef][ISI][Medline]
Kidwell, M. G. 2002. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63.[CrossRef][ISI][Medline]
Knight, C. A., N. A. Molinari, and D. A. Petrov. 2005. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. 95:177–190.
Lachaise, D., M. Harry, M. Solignac, F. Lemeunier, V. Benassi, and M. L. Cariou. 2000. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome. Proc. R. Soc. Lond. B Biol. Sci. 267:1487–1495.[Medline]
Lachaise, D., and J. F. Silvain. 2004. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120:17–39.[CrossRef][ISI][Medline]
Lerat, E., C. Rizzon, and C. Biémont. 2003. Sequence divergence within transposable element families in the Drosophila melanogaster genome. Genome Res. 13:1889–1896.
Li, Y. J., Y. Satta, and N. Takahata. 1999. Paleo-demography of the Drosophila melanogaster subgroup: application of the maximum likelihood method. Genes Genet. Syst. 74:117–127.[CrossRef][ISI][Medline]
Lozovskaya, E. R., D. I. Nurminsky, D. A. Petrov, and D. L. Hartl. 1999. Genome size as a mutation-selection-drift process. Genes Genet. Syst. 74:201–207.[CrossRef][ISI][Medline]
Ma, J., and J. L. Bennetzen. 2004. Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl. Acad. Sci. USA 101:12404–12410.
Ma, J., K. M. Devos, and J. L. Bennetzen. 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14:860–869.
McDonald, J. F. 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10:123–126.
Montchamp-Moreau, C., S. Ronsseray, M. Jacques, M. Lehmann, and D. Anxolabéhère. 1993. Distribution and conservation of sequences homologous to the 1731 retrotransposon in Drosophila. Mol. Biol. Evol. 10:791–803.[Abstract]
Moriyama, E. N., D. A. Petrov, and D. L. Hartl. 1998. Genome size and intron size in Drosophila. Mol. Biol. Evol. 15:770–773.[ISI][Medline]
Nardon, C., G. Deceliere, C. Loevenbruck, M. Weiss, C. Vieira, and C. Biémont. 2005. Is genome size influenced by colonization of new environments in Dipteran species? Mol. Ecol. 14:869–878.[CrossRef][Medline]
Nardon, C., M. Weiss, C. Vieira, and C. Biémont. 2003. Variation of the genome size estimate with environmental conditions in Drosophila melanogaster. Cytometry 55:43–49.[Medline]
Pagel, M., and R. A. Johnstone. 1992. Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox. Proc. R. Soc. Lond. B Biol. Sci. 249:119–124.[Medline]
Parsch, J. 2003. Selective constraints on intron evolution in Drosophila. Genetics 165:1843–1851.
Petrov, D. A. 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17:23–28.[CrossRef][ISI][Medline]
Petrov, D. A., E. R. Lozovskaya, and D. L. Hartl. 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384:346–349.[CrossRef][Medline]
Rizzon, C., E. Martin, G. Marais, L. Duret, L. Ségalat, and C. Biémont. 2003. Patterns of selection against transposons inferred from the distribution of Tc1, Tc3 and Tc5 insertions in the mut-7 line of the nematode Caenorhabditis elegans. Genetics 165:1127–1135.
SanMiguel, P., A. Tikhonov, Y. K. Jin et al. (11 co-authors). 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768.
Sherwood, S. W., and J. L. Patton. 1982. Genome evolution in pocket gophers (genus Thomomys). II. Variation in cellular DNA content. Chromosoma 85:163–179.[CrossRef][ISI][Medline]
Shirasu, K., A. H. Schulman, T. Lahaye, and P. Schulze-Lefert. 2000. A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 10:908–915.
Singh, N. D., and D. A. Petrov. 2004. Rapid sequence turnover at an intergenic locus in Drosophila. Mol. Biol. Evol. 21:670–680.
Strachan, T., E. Coen, D. Webb, and G. Dover. 1982. Modes and rates of change of complex DNA families of Drosophila. J. Mol. Biol. 158:37–54.[CrossRef][ISI][Medline]
Tamura, K., S. Subramanian, and S. Kumar. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21:36–44.
Uozu, S., H. Ikehashi, N. Ohmido, H. Ohtsubo, E. Ohtsubo, and K. Fukui. 1997. Repetitive sequences: cause for variation in genome size and chromosome morphology in the genus Oryza. Plant Mol. Biol. 35:791–799.[CrossRef][ISI][Medline]
Vieira, C., D. Lepetit, S. Dumont, and C. Biémont. 1999. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol. Biol. Evol. 16:1251–1255.[Abstract]
Vieira, C., C. Nardon, C. Arpin, D. Lepetit, and C. Biémont. 2002. Evolution of genome size in Drosophila. Is the invader's genome being invaded by transposable elements? Mol. Biol. Evol. 19:1154–1161.
Vinogradov, A. E. 1999. Intron-genome size relationship on a large evolutionary scale. J. Mol. Evol. 49:376–384.[CrossRef][ISI][Medline]
Warren, A. M., and J. M. Crampton. 1991. The Aedes aegypti genome: complexity and organization. Genet. Res. 58:225–232.[ISI][Medline]
Wendel, J. F., R. C. Cronn, J. S. Johnston, and H. J. Price. 2002. Feast and famine in plant genomes. Genetica 115:37–47.[CrossRef][ISI][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||