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Evidence for Selection at the fused1 Locus of Drosophila americana
Jorge Vieiraa, Bryant F. McAllisterb, and Brian Charlesworthaa Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
b Department of Biology, University of Texas, Arlington, Texas 76019-0498
Corresponding author: Jorge Vieira, Departamento de Genética Molecular, Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, Porto 4150-180, Portugal., jbvieira{at}ibmc.up.pt (E-mail)
Communicating editor: G. B. GOLDING
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX LITERATURE CITED |
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We analyze genetic variation at fused1, a locus that is close to the centromere of the X chromosome-autosome (X/4) fusion in Drosophila americana. In contrast to other X-linked and autosomal genes, for which a lack of population subdivision in D. americana has been observed at the DNA level, we find strong haplotype structure associated with the alternative chromosomal arrangements. There are several derived fixed differences at fused1 (including one amino acid replacement) between two haplotype classes of this locus. From these results, we obtain an estimate of an age of 
0.61 million years for the origin of the two haplotypes of the fused1 gene. Haplotypes associated with the X/4 fusion have less DNA sequence variation at fused1 than haplotypes associated with the ancestral chromosome arrangement. The X/4 haplotypes also exhibit clinal variation for the allele frequencies of the three most common amino acid replacement polymorphisms, but not for adjacent silent polymorphisms. These patterns of variation are best explained as a result of selection acting on amino acid substitutions, with geographic variation in selection pressures.
WHILE the maintenance of polymorphic chromosomal inversions in Drosophila has received much attention (
If this is the case, some genetic differentiation could exist between the different chromosomal arrangements in regions where recombination between the two arrangements is restricted. In D. melanogaster the majority of laboratory-induced X autosome translocations that are viable and fertile are usually broken in the proximal X heterochromatin (1 Mb from the centromeric heterochromatin on chromosome four, these considerations suggest that this might not be true for the base of the X chromosome.
In this context, fused (fu) is a suitable locus for study, since it is located on the X chromosome, 1 Mb away from centromeric heterochromatin (see MATERIALS AND METHODS). This gene encodes a serine-threonine kinase (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX LITERATURE CITED |
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Collection and analysis of chromosomes:
Flies were collected at 10 localities representing a transect through the hybrid zone (
In situ hybridization:
This technique was performed as described by
DNA sequencing and polymorphism analysis:
DNA sequencing of both strands and analyses of DNA polymorphism were performed as described by
It is desirable to use an approach that allows us to directly determine fu1 genomic DNA sequences from single males. We used a pair of primers (FUF and FU4IR; see
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX LITERATURE CITED |
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The organization of DNA sequence variability at fu1:
Genetic differentiation at the fu1 locus may exist between the X/4 fusion chromosome (characteristic of D. a. americana) and the unfused karyotype (characteristic of D. a. texana), since this gene is located in a region where recombination between the two arrangements is likely to be restricted (see Introduction). To examine this question, we initially studied two populations from the northern and southern regions of the range of D. americana, G96 and FP99, representative of D. a americana and D. a. texana, respectively (
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Visual inspection reveals that each sample contains one sequence that is distinct from other sequences in its sample, but very similar to sequences in the other sample. The G96.41 sequence defines 15 additional segregating sites, representing 62.5% of the segregating sites in the G96 sample; the FP99.57 sequence defines 9 additional segregating sites, representing 16.4% of the segregating sites in the FP99 sample. However, only two additional segregating sites are defined by differences between the G96.41 sequence and FP99 sequences (excluding FP99.57), and one by the difference between the FP99.57 and G96 sequences (excluding G96.41). These two sequences are also distinguished by the variants at position 1633 that are very strongly associated with the nonfusion and fusion chromosomes (see below).
It is, therefore, very likely that sequence G96.41 is from a free X chromosome and that sequence FP99.57 is from a fusion X chromosome, given the direct evidence for polymorphism of the fusion within these populations (
Table 1 shows the estimated levels of nucleotide site diversity for the 2.4-kb region of the fu1 locus in the G96 and FP99 samples (discarding the two sequences inferred to belong to the minority karyotypes for these populations, as described above). The level of synonymous DNA polymorphism for the FP99 sample (nonfusion karyotype) is 0.02 per nucleotide site, which is similar to estimates for other genes surveyed in this species (including the X chromosomal locus period), suggesting an effective population size of >106 (10% of that for FP99.
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To determine whether this difference is statistically significant, we generated 10,000 pairs of independent gene trees (
To examine the generality of this observation, DNA sequences of D. americana were also obtained for the HI99, LA99, NN97, and ML97 populations, for a shorter region that corresponds to the first 514 bp of the longer 2.4-kb region analyzed above. Variation at site 1633, which creates a ClaI RFLP marker, defines the two major haplotype classes at the fu1 gene, with haplotypes having C at high frequency in the northern range of D. americana and haplotypes with T in the southern range. As shown in the next section, we can use this information to infer the karyotypes of randomly sampled flies with considerable confidence. On average, four to five individuals were sequenced for each putative karyotype and population analyzed. The haplotype structure of these populations is shown in Fig 2.
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The estimated levels of nucleotide site polymorphism for the region analyzed here are summarized in Table 2. Although there are large variances associated with these diversity estimates, haplotypes with a C at 1633 are generally less variable than haplotypes with a T. This supports our results on the G96 (D. a. americana) and FP99 (D. a. texana) populations for a larger 2.4-kb region of the fu1 gene. The lower variability among northern haplotypes, which are strongly associated with the X/4 fusion (see below), is thus not limited to the G96 population.
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Despite the evidence for considerable gene flow among D. americana populations (
Patterns of geographic variation in karyotypes and DNA sequences:
The results presented above demonstrate significant differentiation between two major haplotype classes at the fu1 locus. The common haplotype class in samples from the northern range of D. americana has a lower level of genetic variability and a higher level of between-population differences in DNA sequences than the common haplotype class in the southern range of D. americana. The geographic distribution of the fu1 haplotypes parallels the distribution of the alternative chromosomal arrangements in D. americana, so that restriction digestion patterns were used to determine the association between the fu1 haplotypes and chromosomal arrangement.
We surveyed five nucleotide site polymorphisms that could be identified by the restriction enzymes ClaI, EaeI, and RsaI in a set of 95 chromosomes from five samples representing a 500-km latitudinal transect exhibiting clinal variation for the X/4 fusion (Table 3). For each of these 95 X chromosomes, identification of its status as fused or unfused to the fourth chromosome was performed by linkage analyses (see MATERIALS AND METHODS). The only variable site for which no significant association was found is site EaeI 107. The other four polymorphic sites surveyed exhibit significant associations with the state of the centromere. The presence of C at the ClaI site 1633, A at the RsaI site 1214, and A at the RsaI site 2157 is always observed for X/4 fusion chromosomes. The data in Table 3 show that the state of the X chromosome would have been erroneously deduced from the ClaI site 1633 in only 3 out of 95 chromosomes, i.e., 3% of the time.
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The close association between the X/4 fusion and the presence of the C variant at the ClaI site 1633 implies that it is possible to estimate the frequency of the former in a given population from the frequency of the latter and to examine the patterns of DNA polymorphism associated with each karyotype. For these purposes, a set of 208 chromosomes from single wild-caught males from several populations, and single males obtained from independent females, was surveyed for ClaI and eight other fu1 polymorphic restriction sites (Table 4 and Table 5; Fig 3 and Fig 4). Most of these polymorphic sites were known to be present in the G96 sample, and this information was used when choosing the five restriction enzymes (EaeI, BbsI, AvaI, RsaI, and ClaI) used in this survey. This set of chromosomes partially overlaps the set of 95 chromosomes analyzed above, but the genetic information about their fusion status was not used in the following analyses.
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No statistically significant differences from 
2 tests are observed between direct and indirect estimates of fusion frequencies throughout the range of the X/4 fusion cline (Table 4). There is, however, a 13% discrepancy between the two estimates for the HI99 sample; the indirect estimate is outside the 95% confidence limit for the direct estimate. The direct estimate of the frequency of the X/4 fusion is significantly correlated both with latitude and longitude (stepwise regression: N = 6; R2 = 0.99; P < 0.001), while the indirect estimate (based on the frequency of the variant at site 1633) is significantly correlated only with latitude (N = 8; R2 = 0.93; P < 0.001). This difference may reflect the lack of complete association of site 1633 with karyotype.
The haplotypes for the 208 chromosomes are shown in Table 5, which is arranged so that the haplotypes of chromosomes inferred to be fusion or nonfusion from the state of their ClaI 1633 site are in the top and bottom sections, respectively. Fig 3 and Fig 4 show the frequency of RFLP variants and RFLP haplotypes in several D. americana populations for individuals that were inferred to carry a X/4 fusion or nonfusion chromosome, respectively. Only those sites for which the variant is represented more than once in the sample of chromosomes being considered are shown (see Table 5). Visual inspection of Fig 3 suggests that there is clinal geographic variation in nucleotide variant frequencies, not only for the AvaI site 442 but also for sites BbsI 1609 and RsaI 2157. These are the three most common replacement polymorphisms present in the G96 sample (see Fig 1).
Stepwise regression analyses reveal significant correlations between latitude and longitude and the variants AvaI 442 (R2 = 0.92; P < 0.005), BbsI 1609 (R2 = 0.88; P < 0.01), RsaI 2157 (R2 = 0.95; P < 0.001), haplotype B (R2 = 0.90; P < 0.005), and haplotype F (R2 = 0.88; P < 0.01). Haplotypes B and F (see Table 5) include the RFLP variants AvaI 442, BbsI 1609, and RsaI 2157. In contrast, no obvious clines are found for silent sites or among nonfusion chromosomes.
In addition, for chromosomes carrying the X/4 fusion, we calculated FST values between the group of northern populations (NN97, C96, G96, and HI99) and the group of southern populations (PM99, LA99, AA99, and FP99) for each of the polymorphic sites in Table 5 (FST values are 0.005, 0.146, 0.012, 0.021, 0.029, 0.133, and 0.021 for sites 107, 442, 1012, 1214, 1609, 2157, and 2187, respectively). The three highest FST values are for the replacement polymorphisms (sites 442, 1609, and 2157). This difference between silent and replacement variants is significant (P < 0.05; Mann-Whitney U-test), showing that differentiation betweeen the northern and southern populations is mainly due to the replacement variants.
Evidence for recombination:
As noted in the Introduction, the location of fu1 near the centromeric heterochromatin of the X chromosome implies that it may be located in a region of reduced crossing over, and that crossing over between fu1 and the centromere may be suppressed in heterozygotes for fusion and nonfusion chromosomes (see the Introduction). In this section we summarize the evidence for recombination at fu1 between unfused and fused chromosomes, within nonfusion chromosomes, and within chromosomes with the X/4 fusion.
If we assume that the X/4 fusion was derived through a single mutational event, some recombination (either gene conversion or crossing over) must have occurred between unfused and fused chromosomes, since there are at least two shared polymorphisms, EaeI 107 and RsaI 2187 (see Table 3). Furthermore, Table 5 shows that haplotypes G, H, O, and P all have a variant that is present once in the sample (at positions 2187, 1214, 442, and 1609, respectively), but which is commoner among the alternative chromosome arrangement. It is likely, therefore, that these haplotypes are the result of crossing over or gene conversion events between nonfusion and fusion chromosomes.
From the FP99 sequence data on nonfusion chromosomes, a minimum of six recombination events can be inferred to have occurred within the fu1 gene (2 tests) is detected only between 8 pairs of sites out of 120 pairwise comparisons. The rate of intragenic recombination, C = 
(where Ne is the effective population size for X chromosomal loci and c is the recombination frequency per nucleotide site in females), was estimated from the variance in the number of differences between pairs of DNA sequences (
= 1.7, where the value of the 
estimator (
From the G96 sequence data on putative X/4 fusion chromosomes (Fig 1), a minimum of one recombination event is inferred to have occurred (2 test, P < 0.05) linkage disequilibrium is only detected between sites 54 and 1343 and 442 and 2157, out of 15 pairwise comparisons. None of these are significant after a Bonferroni correction, except for the association between sites 54 and 1343. From these data we estimate C = 0.11 between adjacent nucleotide sites (the value of C/ is 50, where is for synonymous sites), but it should be noted that this estimate has a large sampling variance. There is only limited evidence for recombination in the other data sets (data not shown).
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX LITERATURE CITED |
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The results described above yield the following main conclusions, which require interpretation in terms of the evolutionary forces affecting the X/4 fusion and the molecular variants at the fu1 locus.
- There are two divergent allelic classes at the fu1 locus, and these are strongly associated with fusion and nonfusion X chromosomes.
- The fusion chromosomes show much less variability at fu1 than nonfusion chromosomes.
- Within fusion chromosomes, there is clinal variation with respect to replacement but not silent site polymorphisms.
Testing for a selective sweep of the fusion chromosome:
At first sight, the simplest interpretation of observations 1 and 2 is that the fusion chromosome originated as a single mutation, which rapidly increased in frequency, causing a loss of variability at the fu1 locus among gametes carrying the fusion because of its close linkage to the centromere; i.e., there has been a selective sweep of the fusion (
We note first that the inferred derived states of the replacement site 1633, which shows a fixed difference between fusion and nonfusion chromosomes in these data, and all six synonymous fixed sites are associated with the fusion chromosome. This was deduced from comparisons with an outgroup sequence from D. montana, which shared a common ancestor with D. americana 10 mya (
We can ask if this asymmetry in the distribution of derived fixed variants between the fusion and nonfusion chromosomes can be accounted for by the selective sweep model. If we assume that the level of polymorphism of the ancestral population was the same as in the nonfusion chromosomes of the FP99 sample, and that the selective sweep involved a single randomly chosen X chromosome, we can estimate the expected number of variants captured by the fusion chromosomes and which are absent from the sample of nonfusion FP99 chromosomes (see the Appendix). The estimated value of for all synonymous sites, based on the number of segregating sites in this sample, is 11.76 (Table 1); on this basis, only 1.18 apparent fixed differences are expected between fusion and nonfusion sequences in these samples (the 95% upper bound from the Poisson distribution is 3). Even if we use the highest true value of , which generates an estimated value as low as 11.76 with probability 5% (18.6, assuming independence between sites and the resulting Poisson distribution:
A single hitchhiking event cannot, therefore, explain all six derived synonymous fixed differences at fu1 between the G96 (fusion) and FP99 (nonfusion) sequences. But the data might, in principle, be compatible with a single selective sweep involving the fusion chromosomes, followed by a period of neutral evolution that allows the accumulation of fixed differences, in addition to those associated with the spread of the fusion. The fixation of a small number of variants in association with the sweep would then remove the apparent paradox that all the fixed differences are associated with the fusion chromosomes, and none with the nonfusion chromosomes; for example, four fixations in one lineage and none in the other are not statistically different from the expectation of two fixations in each lineage.
This raises the question of whether other aspects of the data can be reconciled with this possibility. An estimate of the age of the X/4 fusion from the numbers of fixed synonymous differences between the G96 fusion and FP99 nonfusion chromosomes can be obtained as follows. The above considerations suggest that, at most, three of the six differences are likely to have been associated with a selective sweep of the X/4 fusion. A total of 488 synonymous sites were analyzed from the data in Fig 1, giving a synonymous site substitution frequency of at least 6.1 x 10-3 per site. Assuming a neutral mutation rate of 10-2/site/million years (0.61 million years (with a lower 95% limit of 0.27 million years) for the origin of this chromosome from the ancestral population of nonfused chromosomes. The putative sweep of the fusion is unlikely to be more recent than 0.27 mya.
We can now ask whether the observed low level of variation within the G96 fusion chromosomes is compatible with a selective sweep that occurred 0.27 mya. This can be done very simply by modifying a standard coalescent simulation ( value of 0.02 per site is appropriate for X-linked synonymous sites in D. americana; this is twice the expected number of mutations per unit of coalescent time (2Ne generations). Using the above mutation rate estimate of 2 x 10-8 per year, this yields an estimate of the coalescent time of 0.89 million years. The minimum time of the sweep of the X/4 fusion estimated above (0.27 million years) is thus 0.3 units of coalescent time. By placing mutations onto simulated trees truncated at this point, from a Poisson distribution with mean of 0.5 in units of coalescent time, we can determine the expected distribution of the number of segregating sites. With the 488 synonymous sites surveyed at the fu1 locus, the per locus mutation rate in units of coalescent time is 4.88. Three synonymous polymorphisms were observed among the 10 G96 fusion chromosomes. Among 10,000 replicate simulations with these parameters, only 2.6% have as few or fewer segregating sites as observed. Given the conservative assumptions involved in this calculation, this effectively rules out a single selective sweep of the X/4 fusion as an explanation of the data, if it is assumed that the postsweep effective size of the fusion chromosomes is similar to that of the nonfusion chromosomes.
Other hypotheses:
These results are, however, compatible with the possibility that the fusion chromosomes have persisted for a long time at a low effective population size, either because of a restricted geographical distribution or because subsequent hitchhiking events took place within the fusion chromosomes, due to the spread of alleles that were favored only in the genetic background or geographical location of the fusion chromosomes. Such hitchhiking events would not change the mean substitution rate of neutral alleles (
There are, in fact, features of the data that suggest that selection on amino acid variants has been operating at fu1, which may be relevant to the last hypothesis. In the first place, we note that, although most fu1 variants are strongly associated with the state of the X/4 centromere, the associations are not perfect (Table 3), and that (as described above) there is direct evidence from the data in Fig 2 for recombination between sequences derived from the two chromosome types. In particular, some fusion chromosomes carry variants derived from the nonfusion chromosomes. This weakens the case for a long period of purely neutral evolution with complete isolation between the two chromosomal arrangements.
In addition, all fusion chromosomes surveyed carry a mutation of methionine to a derived threonine at the ClaI site 1633 of fu1, whereas the unfused chromosomes mostly carry the ancestral state. It is possible that this amino acid replacement is advantageous in the "americana" background or in the ecological conditions prevailing in more northerly areas, so that a selective sweep associated with it may have contributed to the reduced variability at fu1 among the fusion chromosomes. Selection maintaining this difference in amino acid sequence would reduce effective gene flow between arrangements and hence elevate divergence at linked silent sites (
There is also a striking difference between the fusion and nonfusion chromosomes in the level of replacement vs. silent polymorphism. The results shown in Table 1 indicate 4 replacement and 5 silent polymorphisms within fusion chromosomes, and 6 replacement and 37 silent polymorphisms within nonfusion chromosomes; this pattern is significant at the 2% level on a 2 x 2 2 test. While it is possible that this could be explained by reduced effective size of the fusion chromosomes, leading to relaxed selection against replacement mutations in the population carrying fusions, such a reduction would be expected to have a bigger effect on the ratio of replacement to silent changes between arrangements compared to the ratio for within-arrangement polymorphisms (
Furthermore, among chromosomes with the X/4 fusion, there are significant correlations between latitude and longitude and the frequencies of the three most common amino acid polymorphisms (at positions 442, 1609, and 2157), as well as for two haplotypes that include these (haplotypes B and F; see Table 5). All three replacement variants are derived and are likely to be younger than the X/4 fusion since they are common only in chromosomes with the X/4 fusion. In contrast, there is no evidence for clinal patterns for silent variants within the fusion chromosomes, and the replacement variants show significantly higher divergence as measured by FST. This suggests that these apparent clines are the result of differential selection pressures in different parts of the species range, in combination with limited gene flow (
Conclusions:
Overall, the fu1 data are consistent with the hypothesis of at least one selective sweep in the americana lineage. There are two likely targets of selection for such a selective sweep. First, the presence of a wide frequency cline for the X/4 fusion (B. F. MCALLISTER, unpublished data) suggests that weak selection is maintaining it (
| ACKNOWLEDGMENTS |
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We thank B. Golding, C. P. Vieira, and an anonymous reviewer for helpful comments on this work. J.V. is supported by the Fundação para a Ciencia e Tecnologia (PRAXIS XXI/BPD/14120/97) and B.C. by the Royal Society. This work was partially supported by the Office of Research and Graduate Studies at the University of Texas at Arlington.
Manuscript received September 25, 2000; Accepted for publication February 2, 2001.
| APPENDIX |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX LITERATURE CITED |
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There is probability x that a randomly chosen gamete from a population contains a variant that is present in the population at frequency x. Thus the probability that a site present at frequency x is absent from a sample of nonfusion chromosomes of size n, giving rise to an apparent fixed difference between the fusion and nonfusion chromosomes, is (1 - x)n, in the absence of exchange at fu1 between the two chromosomal arrangements. In a population at equilibrium under the infinite sites neutral model, the expected number of sites with a derived variant at frequency x is x-1 ( is the product of 4Ne (Ne is the effective population size for X chromosomal loci) and the neutral mutation rate u for the region in question. Assuming independence between sites, as is justified by the low level of linkage disequilibrium detected in the FP99 sample (see RESULTS), if N is the size of the ancestral population, the expected number of variants captured by the fusion chromosome that are absent from the D. a. texana sample is
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B. F. McAllister Sequence Differentiation Associated With an Inversion on the Neo-X Chromosome of Drosophila americana Genetics, November 1, 2003; 165(3): 1317 - 1328. [Abstract] [Full Text] [PDF]
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 A. Navarro-Sabate, M. Aguade, and C. Segarra Excess of Nonsynonymous Polymorphism at Acph-1 in Different Gene Arrangements of Drosophila subobscura Mol. Biol. Evol., November 1, 2003; 20(11): 1833 - 1843. [Abstract] [Full Text] [PDF]
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C. P. Vieira, P. A. Coelho, and J. Vieira Inferences on the Evolutionary History of the Drosophila americana Polymorphic X/4 Fusion From Patterns of Polymorphism at the X-Linked paralytic and elav Genes Genetics, August 1, 2003; 164(4): 1459 - 1469. [Abstract] [Full Text] [PDF]
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 A. Navarro and N. H. Barton Chromosomal Speciation and Molecular Divergence--Accelerated Evolution in Rearranged Chromosomes Science, April 11, 2003; 300(5617): 321 - 324. [Abstract] [Full Text] [PDF]
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J. Vieira Two Divergent Species of the Virilis Group, Drosophila littoralis and Drosophila virilis, Share a Replacement Polymorphism at the fused Locus Mol. Biol. Evol., April 1, 2002; 19(4): 579 - 581. [Full Text] [PDF]
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