MBE Advance Access originally published online on December 10, 2007
Molecular Biology and Evolution 2008 25(2):409-416; doi:10.1093/molbev/msm269
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Research Articles |
Selective Sweeps in a 2-Locus Model for Sex-Ratio Meiotic Drive in Drosophila simulans
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* Ecole Pratique des Hautes Etudes, Paris, France
Laboratoire Evolution Génome et Spéciation, UPR9034, CNRS 91198 Gif-sur Yvette Cedex, France
Département de biologie Université Paris-Sud 11, 91405 Orsay Cedex, France Gif-sur-Yvette, France
Ecologie, Systématique et Evolution, CNRS UMR8079, Université Paris-Sud 11, 91405 Orsay, France
E-mail: veuille{at}mnhn.fr.
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Abstract |
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A way to identify loci subject to positive selection is to detect the signature of selective sweeps in given chromosomal regions. It is revealed by the departure of DNA polymorphism patterns from the neutral equilibrium predicted by coalescent theory. We surveyed DNA sequence variation in a region formerly identified as causing "sex-ratio" meiotic drive in Drosophila simulans. We found evidence that this system evolved by positive selection at 2 neighboring loci, which thus appear to be required simultaneously for meiotic drive to occur. The 2 regions are approximately 150-kb distant, corresponding to a genetic distance of 0.1 cM. The presumably large transmission advantage of chromosomes carrying meiotic drive alleles at both loci has not erased the individual signature of selection at each locus. This chromosome fragment combines a high level of linkage disequilibrium between the 2 critical regions with a high recombination rate. As a result, 2 characteristic traits of selective sweeps—the reduction of variation and the departure from selective neutrality in haplotype tests—show a bimodal pattern. Linkage disequilibrium level indicates that, in the natural population from Madagascar used in this study, the selective sweep may be as recent as 100 years.
Key Words: meiotic drive • sex ratio • selective sweep • Drosophila simulans
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Genetic interactions have been at the heart of evolutionary thinking ever since Wright made it the focus of his contribution to the foundation of theoretical population genetics (Wright 1931
). As adaptation is detected in an increasing number of molecular sequence data sets, it is, however, apparent that DNA variation at the population level has hitherto been investigated in only a few systems of interacting genes (Palopoli and Wu 1996; Zapata et al. 2002; Caicedo et al. 2004; Takano-Shimizu et al. 2004). A reliable framework exists for detecting the molecular signature of positive selection (selective sweep) in isolated genes, based on the hitchhiking theory (Maynard-Smith and Haigh 1974) and its adaptation to coalescent theory (Kaplan et al. 1989). Departure from neutrality using a series of statistical tests based on the distribution of mutations (Hudson et al. 1987; Tajima 1989; Fu and Li 1993; Fay and Wu 2000) and haplotypes (Hudson et al. 1994; Kirby and Stephan 1995; Depaulis and Veuille 1998) has been identified in a number of molecular sequences and used to map putatively adaptive mutations (Hudson et al. 1994; Depaulis et al. 1999; Rozas et al. 2001; Glinka et al. 2003; DuMont and Aquadro 2005).
Here we report a case of selective sweep involving interactions between 2 neighboring loci contributing to "sex-ratio" meiotic drive in Drosophila simulans (Montchamp-Moreau et al. 2006). Meiotic drive is a process whereby some chromosomes or alleles, when heterozygous, can "hijack" reproductive cells in favor of their own transmission (Novitski and Sandler 1957). The evolution of meiotic drive systems is determined by 2 remarkable features. First, it results from nonadaptive selection because driver alleles are selfish elements capable of spreading in populations even if they are deleterious (provided their preferential transmission in gametes exceeds their fitness cost). Second, meiotic drive systems are famous examples of gene interaction between driver elements and their target locus. The different elements contributing to the drive tend to evolve as a single genetic unit because this maximizes their selective advantage (Crow 1991). Recombination-inhibiting mechanisms, such as chromosome inversions, are the rule in previously studied systems (Lyttle 1991; Jaenike 2001). They have put a limit on genetic analysis and the full development of population genetics studies.
The sex-ratio system described in some oceanic islands and African populations of D. simulans (Atlan et al. 1997) is an exception to the rule. It consists of driver elements located in a freely recombining region of the X chromosome (Cazemajor et al. 1997). They act in male individuals and cause the nondisjunction of Y chromosomes at meiosis (Cazemajor et al. 2000). A male carrying a sex-ratio X chromosome (XSR) together with its Y mostly transmits XSR, producing a majority of female in its offspring. An initial mapping study led us to record sequence variation at the Nrg gene. This revealed a selective sweep associated with the spread of XSR chromosomes in 2 natural populations from the Indian Ocean, Madagascar, and Réunion, where about one-half of the X chromosomes were sex-ratio at the time of the sampling. (Derome et al. 2004). Cytogenetic studies showed that XSR chromosomes are characterized by the presence of an approximately 30-kb tandem duplication, whereas a comparison with the annotated genome of the closely related Drosophila melanogaster suggests this duplication to contain 6 genes (Montchamp-Moreau et al. 2006). Genetic mapping showed that the duplication is necessary but not sufficient to cause a drive. All those experiments involved the recombination of an XSR chromosome into a standard chromosome. The points of recombination were mapped using molecular markers and ranked for an increasing invasion of the XSR chromosome into the standard chromosome from the telomeric end toward the centromeric end and vice versa for the complementary experiment. The 2 complementary experiments did not converge to the same point, as summarized in figure 1. When invading distally from the centromere, the XSR chromosome determined a sex-ratio phenotype only after bypassing what later appeared to be the duplication. When invading proximally from the telomere, it determined a stable sex-ratio phenotype only after crossing a region approximately 150-kb distant from the duplication (Montchamp-Moreau et al. 2006). It thus appeared that the trait required at least the presence of a second element located approximately 150 kb proximally from the duplication. However, it could not be determined whether the intervening region between these limits was required to induce a drive.
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77% of females). When it invades from the C end (lines C1 and C2), the sex-ratio phenotype appears after the recombinant zone has crossed the duplication (adapted from Derome et al. 2004To further characterize this region and the underlying selective mechanisms, we used the same sample of X chromosomes from Madagascar as in Derome et al. (2004)
. We document DNA sequence variation in 12 DNA fragments distributed over approximately 200 kb, covering the entire zone shown in figure 1. Sequence polymorphism analysis clearly shows the signature of selective sweeps in 2 gene regions that are involved in the sex-ratio drive and brings indisputable evidence that driver alleles in both regions were the targets of the selective process. Our results then demonstrate the role of gene interactions in the evolution of this molecular system. |
Materials and Methods |
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Chromosome Sample and Molecular Markers
We used the previously investigated random sample of 10 XSR and 5 XST chromosomes from Madagascar (Derome et al. 2004
; Montchamp-Moreau et al. 2006). Introducing each of the XSR chromosomes into a reference suppressor-free genetic background produced progenies with the following proportions of females: XM01: 86%; XM02: 91%; XM04: 92%; XM06: 84%; XM07: 84%; XM08: 92%; XM09: 93%; XM12: 90%; XM14: 71%; and XM15: 85%. Using the annotated D. melanogaster sequences (GenBank accession numbers AE003443 and AE03444), we selected 11 fragments covering an approximately 200-kb genomic region. Their sizes ranged between 354 and 1,054 bp (supplementary fig. S1, Supplementary Material online). Oligonucleotides for polymerase chain reaction (PCR) amplification and sequencing are given in supplementary table S1 (Supplementary Material online). They were designed from genes of the D. melanogaster sequence and corrected when appropriate by comparison with the publicly available D. simulans sequence at the Genome Sequencing Center at Washington University—School of Medicine, http://genome.wustl.edu/.
Marker design took into account 3 main requirements. Primers were preferentially taken from coding regions to optimize locus-specific priming, intervening sequences encompassed preferentially silent sites (e.g., introns) to maximize variation, and finally, markers were as evenly spaced as possible in the studied area. Because the D. simulans genome-sequencing project was not completed for this part of the X when we initiated our work, we used the coding genes of the D. melanogaster genome as hypothetical landmarks of the D. simulans genome. This approach proved valid because later results showed synteny between the 2 genomes and comparable size of the 2 homologous regions.
Analysis of Sequence Polymorphism Data
Extraction of genomic DNA from a single male, PCR amplification, and direct sequencing or cloning of PCR product were carried out as previously described (Derome et al. 2004). DNA sequences were manually aligned. Sequences were assigned to either of the duplicates by retaining the order which minimized the number of recombination events following the duplication event, while remaining compatible with the positions inferred from recombination-mapping studies performed with XSR6 (Montchamp-Moreau et al. 2006).
The DnaSP program, version 4.1 (Rozas and Rozas 1999), and the Allelix program (Mousset et al. 2003) were used to estimate molecular variation parameters and to perform neutrality tests. For tests with recombination, we used the experimentally derived genetic distance of c = 7.7 ± 2.6 cM in the "lozenge-singed" region (Derome et al. 2004). The number of nucleotides between these 2 genes is not exactly determined. Assuming that it is the same as in the closely related D. melanogaster (1.3 Mb), this recombination rate would correspond to a value of c = 5.9 x 10–8 recombination event per base pair in females or r = 4 x 10–8 (two-third of this value) in the population as a whole, owing to the fact that there is no recombination in male Drosophila. The neighbor-joining trees were built using the program MrEnt v1.2 of Zuccon A. and Zuccon D. (2006).
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Results |
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A total of 194 segregating sites and 21 insertion/deletion polymorphisms were detected across the 12 sequenced fragments in the sample of 10 XSR and 5 standard (XST) chromosomes from Madagascar. The fragments, named A through L in alphabetic order, correspond to the following genes: CG10555, Trf2, CG1440, CG12123, org-1, Cp36, Nrg (2 sequences), CG11265, CG2056, CG12065, and Crag (supplementary table S1, Supplementary Material online). Four of these genes overlap the sex-ratio duplication; the 8 corresponding fragments are named B, C, D, and E and Bd, Cd, Dd, and Ed for the original and duplicated copies, respectively. The raw sequence alignment (supplementary fig. S2, Supplementary Material online) is converted into an alignment of haplotypes (fig. 2). We found no trace of duplication on the XST chromosomes. The superimposition of 2 sequences in some sequencing runs of fragments B, C, D, or E from the 10 XSR chromosomes confirmed that the 4 loci were duplicated—as previously shown by in situ hybridization (Montchamp-Moreau et al. 2006
)—and, in these cases, did not harbor identical sequences. When a single sequence was detected in some fragments of an XSR chromosome, as confirmed by multiple cloning of PCR products, we assumed the corresponding gene to be duplicated and the 2 copies to be identical. This seems reasonable because a previous study of XSR6 (Montchamp-Moreau et al. 2006) demonstrated that this chromosome carries the same sequences at C and Cd and at D and Dd. When 2 sequences were identified, figure 2 shows the most plausible interpretation of the alignment of haplotypes (see Materials and Methods). The location of loci on the genetic map and a neighbor-joining tree illustrating genetic relatedness between haplotypes is shown in figure 3.
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The essential result was that variation was highly structured into 2 categories of marker loci. A major haplotype of between 9 and 12 sequences with 100% similarity distinctly appeared in 12 loci, whereas all other haplotypes were found only once. This pattern involved the 2 sets of the 4 duplicated loci (B, C, D, and E and Bd, Cd, Dd, and Ed in fig. 2, hereafter BCDE) and also another group of 4 contiguous loci (H, I, J, and K in fig. 2, hereafter HIJK). The 2 extreme loci (A and L) and the 2 intermediate ones (F and G) were more variable, with a major haplotype never representing more than 6 sequences. The 2 groups with reduced variation (BCDE and HIJK) were in significant linkage disequilibrium within each group and between either group (table 1). They showed significant association of the major haplotype with the sex-ratio phenotype, except for K. There is a distinct lack of variation of the XSR chromosomes in the BCDE–HIJK clusters of loci. This appears in figure 4, where nucleotide variation in XSR chromosomes (estimated from Tajima's
) is compared with nucleotide variation in XST chromosomes. The outer limits of these 2 clusters correspond to the limits of the region identified in recombinant studies as being required for the expression of the sex-ratio phenotype. These points are located distally between A and B and proximally between K and L. They are 160–190 kb apart, as estimated from the D. melanogaster genetic map (without the duplication).
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The other 4 loci showed either 1 (L), 2 (F), or 3 (A, G) intermediate frequency haplotypes, the other haplotypes being found only once. Two of these loci (G and L) were in linkage disequilibrium with some loci from the BCDE and HIJK clusters and, thus, could not be formally excluded from the region affected by the selective sweep. In order to investigate this point, selective neutrality tests were run on the data (table 2). The H-test of Depaulis and Veuille (1998)
was significant at loci B, E, H, I, J, and K, that is, only in loci from the BCDE and HIJK clusters. The H-test is a one-tailed test that compares haplotype diversity with the lower limit of its expectation based on the number of polymorphic mutations. The power of the test depends on the absolute number of observed mutations and, thus, may vary over loci. In this case, we ran the test assuming a recombination rate of zero, which is conservative, because recombination tends to increase the number of haplotypes. Tajima's D and the Fay and Wu statistics were nonsignificant, which is not unexpected because these tests have limited power in detecting partial selective sweeps (Depaulis et al. 2003; Mousset et al. 2004).
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The power of the H-test is enhanced by the fact that the major haplotype has undergone no new mutations since the last selective event, which thus leads to the conclusion that this event is very recent. Some sequences seem to result from recombination or gene conversion between the major haplotype and other sequences. We observed no sequences that could have derived from the major haplotype by one or a few point mutations. The sequences closest to the major haplotype always departed from it by nucleotide changes that were also present in a third haplotype. Because nucleotide diversity was never above 3% in the studied set of loci, the probability of 2 mutations occurring independently at the same site and giving the same nucleotide is negligible. Therefore, any change showing such a pattern is very unlikely to result from anything else than gene conversion or recombination. The number of sequences carrying the major haplotype decays gradually on the sides of each candidate region. The sequence pattern at markers A, F, G, and L showed several haplotypes at intermediate frequencies, suggesting that recombination disrupted the association between these regions and the sex-ratio candidate loci during a selective sweep event.
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Discussion |
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Characterizing a Double Selective Sweep
Our results show evidence of a strong haplotype structure in a freely recombining region of the X chromosome in a Malagasy population of D. simulans. It consists of 2 clusters of loci. In each locus, a single major haplotype is in complete or nearly complete linkage disequilibrium with the major haplotypes of the other loci (both within and between clusters). Most genes in these clusters (6 out of 8, counting duplicated loci only once) show the signature of a recent partial selective sweep using a haplotype test. In each set, at least one locus (Ed, B, and H) shows complete association with the sex-ratio phenotype and the most distant points in the 2 clusters colocalize with the limits of the region shown to contain distorter elements responsible for drive on the reference sex-ratio chromosome XSR6 (Montchamp-Moreau et al. 2006
).
The pattern of variation in the intervening region between these clusters very likely represents a partial selective sweep at loci that harbor only neutral variation but are linked to neighboring genes harboring positively selected alleles (Mousset et al. 2004). Mapping experiments have shown recombination between XST and XSR chromosomes to occur at a high rate in the whole surveyed region (Montchamp-Moreau et al. 2006). Recombination between the 2 groups of loci before the completion of the selective phase may explain why several haplotypes at loci F and G have reached intermediate frequencies. Recombination between the 2 groups of loci both during and after the selective phase can explain the loose association of those intermediate frequency haplotypes with the selected phenotype (in this case, the sex-ratio meiotic drive). Ultimately, this leads to the conclusion that we are in presence of a double sweep caused by positive selection at 2-drive loci simultaneously. Alternatively, the polymorphism pattern at loci F and G could indicate a more complex history for the region, for instance, which sweeps occurred sequentially in region B–E and H–K. Whatever the scenarios, the BCDE and HIJK clusters, which are genetically more distant from each other than from intervening loci, remain in complete linkage disequilibrium at several loci. This suggests that positive selection linking these distant loci took place very recently.
The sex-ratio tandem duplication overlapped 4 markers in this study. Two XSR chromosomes from Madagascar (XM04 and XM14), as well as the XSR6 from Seychelles, did not carry the major haplotype at several duplicated loci (fig. 2). Consistently, recombination experiments allowed exchanging alleles over a large part of the duplication without inhibiting the meiotic drive (Montchamp-Moreau et al. 2006). The role of the duplication as the causative agent of the drive may thus involve gene dosage rather than allelic identity. Alternatively, it may involve an element that was unaffected by the various recombination events recorded so far. Under the gene dosage hypothesis, the 6 annotated genes included in the duplication (Trf2, CG32712, CG12125, CG1440, CG12123, and org-1) are all plausible candidates because they are expressed in the testes of D. simulans males (Montchamp-Moreau et al. 2006). From a functional point of view, the gene Trf2 (TATA box–binding protein-related factor 2) seems a priori the best candidate: it is essential for premeiotic chromatin condensation and proper differentiation of germ cells in both sexes (Kopytova et al. 2006). Regarding the second element involved in drive, mapping data together with expression data from Montchamp-Moreau et al. (2006) identified 5 possible genes (CG11265, CG12111, CG2056, CG12065, and Crag). The present population study led us to retain CG11265, CG12111, and CG2056 as the most plausible targets of selection because they are located in the region showing the strongest association with the sex-ratio trait (from marker I to marker J). At this point, we cannot interpret the occurrence of 2 "sex-ratio regions" in functional terms as our study relies exclusively on genetic analyses (crossings, mapping, and polymorphism pattern studies).
Results do not suggest that recurrent selective sweeps occur in this region because XST chromosomes show a genetic variation similar to other genes of the X chromosome (supplementary table S2, Supplementary Material online). This is shown by the fact that the average silent genetic variation in the 5 XST chromosomes was 
= 2,143 (standard deviation [SD] = 1,009), whereas in 4 other regions of the X chromosomes for a sample of 12 Madagascar lines (Baudry et al. 2004), this value was = 2,075 (SD = 0.775).
Estimating the Age of the Selective Sweep
In a former study using nucleotide polymorphism in a 774-bp fragment from the same 15 lines (Derome et al. 2004), the age of the selective sweep in Madagascar was estimated to be less than 18,000 years. The new data provide information on 5,618 nucleotides from 12 genes. The mutation rate in this region can be derived from the expected value of Watterson's estimator of the mutation parameter ( = 3Neµ) under neutral equilibrium. We can assume the XST set of chromosomes to be at a neutral equilibrium. The 0.05 probability of no mutation occurring over L nucleotides in t generations in the sex-ratio set of chromosomes can be estimated as e–
= 0.05, where = tµL and L = 53,329 is the number of sequenced nucleotides in the major haplotype. Assuming an effective population size Ne = 106 in D. simulans (Berry et al. 1991) and an average number of 10 generations per year in Madagascar, we find t = 1,182 years. This is an upper limit estimate; because no mutation was observed, the time since the selective sweep can be any value between zero and t.
On the other hand, genetic recombination offers time estimates at a much finer scale. Given the empirical rule that the mutation and recombination rates are of approximately similar magnitude per bp in highly recombining regions of the Drosophila genome, examining recombination between 200-kb distant loci is much more informative than examining mutations over 6 kb of sequenced nucleotides. Because the organization of the BCDE duplicated region is uncertain, we limited this estimation to the HIJK region. Genes in this region have remained in close linkage disequilibrium, even though a perfect match between the sex-ratio phenotype and the major haplotype was lost in some of them. Assuming that the selective sweep initially equalized variation over these 4 genes, linkage disequilibrium would then have been at most D0 = 0.25 (in this calculation, we pooled all nonmajor haplotypes into a single class, simplifying the genetic system as a diallelic case). Afterward, recombination occurred and linkage disequilibrium decreased at a rate Dt = D0 x e–rt from time 0 to time t. Although drive expression is now completely suppressed in the population (Jutier et al. 2004), we cannot exclude the possibility that selective forces tend to hold these genes together. Therefore, the calculation provides a maximum rate of decay, which, in turn, corresponds to a minimum time estimate. The 2 most extreme markers of the HIJK cluster are 38-kb distant on the D. melanogaster map, and this value is assumed to be similar in D. simulans. Linkage disequilibrium between these genes is currently Dt = 0.067 for an estimated recombination rate r = 0.0015 (see Materials and Methods). The estimated time since the selective sweep occurred is therefore t = 877 generations, or 88 years, which is consistent with the estimate obtained from the mutation rate.
Evolution of the Sex-Ratio Drive in the Population Context
Several markers of the duplicated region of the XSR6 reference chromosome from the Seychelles show 100% sequence similarity with the major haplotype from Madagascar. The absence of mutations denotes homology and recency of the sex-ratio systems at both locations. Similarly, the major allele at the Nrg locus in Madagascar is also the major allele found in Réunion (Derome et al. 2004) and Mayotte (Derome N, Montchamp-Moreau C, Veuille M, unpublished results), suggesting that selective sweeps involving a single ancestral XSR chromosome occurred in several islands over a short period of time. In addition, the sequence identity of the major haplotypes between C and Cd, D and Dd, and likely between B and Bd indicates that a consistent part of the duplication was not affected by recombination since its appearance and the subsequent sweep. This, in turn, implies that the duplication itself might be very recent. The absence of similarity of the Malagasy XSR with the Seychelles XSR6 chromosome in the proximal region—including Nrg—indicates, however, that the corresponding determinants of the drive may not be universal and/or may have a more ancient history.
Theoretical studies have shown that the spread of sex-ratio chromosomes in populations induces selective pressures in favor of drive suppressors on the Y chromosome and on the autosomes (Fisher 1930; Hamilton 1967). Both types of suppressors evolved in D. simulans, and sex-ratio distorters are now completely silenced over a large part of Africa, including Madagascar (Atlan et al. 1997). Once kept in check by suppressors, XSR chromosomes can disappear solely by drift or be counterselected due to their deleterious effects. Another possibility is that they counteract suppressors by the recruitment of new modifiers and spread again. However, the pattern of variation found in D. simulans seems to exclude the occurrence of many recurrent events involving the same sex-ratio drive loci in the past because repeated bursts of selective sweeps would have erased any variation in this region. It appears that the sex-ratio drive system found in D. simulans is rather different from those formerly studied in other Drosophila species. Whereas the other examples seem to have a long evolutionary history (Babcock and Anderson 1996; Dyer et al. 2007), the present molecular data suggest that the system in D. simulans is very recent, at least in the surveyed geographic area. This recentness may explain why it lacks recombination-inhibiting mechanisms, the evolution of which is predicted by the theory and observed in most other species (Crow 1991; Jaenike 2001; Dyer et al. 2007).
A valuable property of meiotic drive systems is to provide a qualitative assessment of the selective forces in action that can be checked experimentally in the laboratory. Among them, the sex-ratio system in D. simulans lends itself to genetic mapping and to so-called selective sweep mapping (Schlotterer 2003) due to the absence of recombination-inhibiting mechanisms. A salient fact of the results is that our a priori belief that a sex-ratio system should result in a very strong selective drive is probably erroneous in this case. The strength of selection was not sufficient to erase variation over a large chromosomal region, allowing the intervening sequences to remain independent of the surrounding selected regions and, consequently, allowing the interacting regions to appear as 2 distinct clusters of genes in linkage disequilibrium, emerging from a background of neutral variation.
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Supplementary Material |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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The sequences reported in this paper have been deposited in the European Molecular Biology Laboratory Nucleotide Sequence Database under accession numbers: AM400855 [GenBank] –AM400869 [GenBank] ; AM401589 [GenBank] –AM401613 [GenBank] ; AM401614 [GenBank] –AM401638 [GenBank] ; AM403248 [GenBank] –AM403272 [GenBank] ; AM403273 [GenBank] –AM403297 [GenBank] ; AM403503 [GenBank] –AM403517 [GenBank] ; AM400840 [GenBank] –AM400854 [GenBank] ; AY3211904–AY3211918; AM402400 [GenBank] –AM402414 [GenBank] ; AM402415 [GenBank] –AM402429 [GenBank] ; AM402430 [GenBank] –AM402444 [GenBank] ; AM402385 [GenBank] –AM402399 [GenBank] . Supplementary tables S1 and S2 and figures S1 and S2 are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).
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Acknowledgements |
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This work was supported by annual funding from the Centre National de la Recherche Scientifique (CNRS) to Unité Propre de Recherche 9034 and 5202, funding from the Ecole Pratique des Hautes Etudes, from the Groupement de Recherche CNRS 1928 Population Genomics, and grant from the Agence Nationale de la Recherche (ANR-06-BLAN-0128-02).
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Footnotes |
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1 Present address: Université Laval, Québec, Canada.
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