Molecular Biology and Evolution 18:279-290 (2001)
© 2001 Society for Molecular Biology and Evolution
ARTICLE |
Contrasting Patterns of X-Linked and Autosomal Nucleotide Variation in Drosophila melanogaster and Drosophila simulans
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, Scotland
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Abstract |
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Surveys of molecular variation in Drosophila melanogaster and Drosophila simulans have suggested that diversity outside of Africa is a subset of that within Africa. It has been argued that reduced levels of diversity in non-African populations reflect a population bottleneck, adaptation to temperate climates, or both. Here, I summarize the available single-nucleotide polymorphism data for both species. A simple "out of Africa" bottleneck scenario is consistent with geographic patterns for loci on the X chromosome but not with loci on the autosomes. Interestingly, there is a trend toward lower nucleotide diversity on the X chromosome relative to autosomes in non-African populations of D. melanogaster, but the opposite trend is seen in African populations. In African populations, autosomal inversion polymorphisms in D. melanogaster may contribute to reduced autosome diversity relative to the X chromosome. To elucidate the role that selection might play in shaping patterns of variability, I present a summary of within- and between-species patterns of synonymous and replacement variation in both species. Overall, D. melanogaster autosomes harbor an excess of amino acid replacement polymorphisms relative to D. simulans. Interestingly, range expansion from Africa appears to have had little effect on synonymous-to-replacement polymorphism ratios.
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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Drosophila melanogaster and Drosophila simulans are cosmopolitan sister species that are believed to have an African origin (Lachaise et al. 1988
). The timing of their dispersal from Africa is not known with any certainty, but proposed estimates are tens of thousands of years ago for "ancient populations" such as those of Europe and Asia and as little as several hundred years ago for the Americas (David and Capy 1988
; Lachaise et al. 1988
). Several recent studies of D. melanogaster reveal that non-African populations harbor reduced levels of nucleotide diversity relative to African populations (Hale and Singh 1991
; Begun and Aquadro 1993, 1995
; Schlötterer, Vogl, and Tautz 1997
; Langley et al. 2000
). Similarly, a recent genome-wide study of microsatellite variation in D. simulans (Irvin et al. 1998
) reports reduced variation in non-African populations relative to African populations. Differences between African and non-African populations have been interpreted as reflecting founder events in the history of non-African populations, directional selection for adaptation to temperate habitats, or both (David and Capy 1988
; Begun and Aquadro 1993, 1995
; Irvin et al. 1998
; Langley et al. 2000
). Hereafter, I will refer to the purely demographic hypothesis that only a limited number of African lineages gave rise to non-African populations as the "bottleneck hypothesis."
In D. melanogaster, comparisons of African and non-African levels of nucleotide diversity have focused primarily on the X chromosome (e.g., Begun and Aquadro 1993, 1995
; Langley et al. 2000
). Patterns of polymorphism at these loci suggest a bottleneck in non-African populations. Curiously, the handful of autosomal loci that have been studied (Clark and Wang 1997
; Aguadé 1998, 1999
; Tsaur, Ting, and Wu 1998
; Begun et al. 1999
; Andolfatto and Kreitman 2000
) do not support this hypothesis. The data are more scarce for D. simulans, for which African and non-African single-nucleotide variation has been compared at only two-single copy nuclear loci (Begun and Aquadro 1995
; Hamblin and Veuille 1999
). Here, I reexamine the bottleneck hypothesis for D. melanogaster and D. simulans using single-nucleotide polymorphisms for a large number of loci scattered throughout the genome. While nucleotide variation in these two species has been summarized before (Moriyama and Powell 1996
), a very different picture emerges when African and non-African populations are considered separately.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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Test of the Bottleneck Hypothesis
I compiled the available nucleotide polymorphism data sets for which there were at least two alleles sampled from both African and non-African populations and at least one polymorphism. In(2L)t refers to the sequence spanning the proximal breakpoint of this D. melanogaster inversion (Andolfatto and Kreitman 2000
). The Adh data set encompasses the Adh and Adh-duplicate loci. This sample was a composite of the sample of Kreitman and Hudson (1991)
and unpublished data (Zimbabwe, Africa) kindly provided by S.-C. Tsaur. Inverted chromosomes were excluded for In(2L)t and Adh, since these loci are very close to the In(2L)t proximal breakpoint (Andolfatto and Kreitman 2000
). Adh-Fast chromosomes were excluded, since sampling was not random with respect to this allele. Cec-C (Clark and Wang 1997
) and Amy-d (Inomata et al. 1995
) were chosen as representative genes from their respective clusters to avoid nonindependence issues. Data for Pgi in D. melanogaster and D. simulans (J. McDonald, personal communication) can be found in GenBank under accession numbers 20575–20556, 27539–27539, and 27554–27555. Unpublished data for transformer (R. Kulathinal, personal communication) and su(s) and su(wa) (Langley et al. 2000) were kindly provided by the authors. For su(s) and su(wa), I use the European sample as the non-African sample because combined European–North American data were not available. References for other loci are as follows: anon1A3, anon1E9, and anon1G5 (Schmid et al. 1999
); Acp26Aab (Tsaur, Ting, and Wu 1998
); Acp29AB (Aguadé 1999
); asense (Hilton, Kliman, and Hey 1994
); Boss (Ayala and Hartl 1993
); diptericin (Clark and Wang 1997
); Dras1, Dras2, and Dras3 (Gasperini and Gibson 1999
); eve (Ludwig and Kreitman 1995
); G6pd (Cooke and Oakeshott 1989
; Eanes et al. 1996
); period (Kliman and Hey 1993
); Ref(2)P (Wayne, Contamine, and Kreitman 1996
); Rh3 (Ayala, Chang, and Hartl 1993
); Tpi (Hasson et al. 1998
); transformer (Walthour and Schaeffer 1994
); vermilion (Begun and Aquadro 1995
); and Yp2 and zeste (Hey and Kliman 1993
). Included are data for 41 short expressed sequence tag (EST) markers, labeled in table
1
according to their cytological positions (8 X-linked and 33 autosomal; Teeter et al. 2000
). Other loci from Teeter et al. (2000)
include achaete, Dms, Dop, Fog, frizzled, nina A, numb, swallow, sevenless, Tra2, tailless, thickveins, and Tph. For D. simulans, I used the G6pd data set of Hamblin and Veuille (1999)
and the vermilion data set of Begun and Aquadro (1995)
. I excluded alleles of unknown origin.
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Individual homologous loci were compared in African and non-African samples to account for locus-specific substitution rates and effective population sizes. I considered only two-state single-base substitution variation in these analyses; nucleotide substitutions overlapping with deletions were discarded as incomplete information. I used a measure of nucleotide diversity (
W) based on the total number of segregating sites in a sample proposed by Watterson (1975)
. I included synonymous, replacement, and noncoding polymorphisms in my count of segregating sites. The summary W is expected to be sensitive to changes in population size (Tajima 1989b
). The use of another measure of nucleotide diversity (
; Tajima 1983
) led to similar conclusions.
Sign tests (Sokal and Rohlf 1998
, p. 444) were performed with the null hypothesis that nucleotide diversity levels are equal in non-African and African populations (i.e., that there was no bottleneck). The tests were one-tailed, since, under both the null and alternative (i.e., a bottleneck) hypotheses, we do not expect more variation outside of Africa.
The sign test assumes that loci are independent. It is unclear whether this is strictly true in the case of loci at the tip of the X chromosome in D. melanogaster (i.e., cytological positions 1A to 2B), which are believed to experience little crossing over (reviewed in Langley et al. 2000
). This said, recombination events (cf. Hudson and Kaplan 1985
) could be detected within the su(s) and su(wa) loci. In addition, linkage disequilibrium has been shown to decay with distance at su(s) and su(wa) on the same scale as loci in regions with higher rates of crossing over (Langley et al. 2000
). Evidence for considerable recombination (perhaps gene conversion) in these data suggests that collapsing these loci into a single data point is overly conservative. Nonetheless, if the average of all six loci (weighted equally) was used as a single data point, the qualitative conclusions were unchanged.
Levels of Nucleotide Diversity by Chromosome and Geographic Locality
I compared diversities at loci in African and non-African populations of D. melanogaster and D. simulans. Average X and autosome synonymous site diversities (W and ) included only synonymous sites of coding regions (i.e., all noncoding sites and loci were excluded). I report mean synonymous site diversities over all loci, weighting each of the loci equally. This weighting was not entirely appropriate, since sequenced loci varied in length and sample size, and population samples were not drawn identically. Unfortunately, this problem is inherent in analyses that combine data from many sources. I excluded the data of Teeter et al. (2000)
from calculations of nucleotide diversity, since many of the loci are very short (i.e., less than several hundred base pairs) and original sequences were not available for the assignment of coding regions. DnaSPv3.0 (Rozas and Rozas 1999
) was used for polymorphism analyses.
In comparisons of averages of nonhomologous loci, I wished to minimize the effects that the recombinational landscape of each chromosome may have on levels of nucleotide variation (Aquadro, Begun, and Kindahl 1994
; Charlesworth 1996
). To this end, I excluded anon1E9, asense, and Dras1 from diversity calculations for D. melanogaster. Synonymous variation at these loci was more likely to be affected by selection at linked sites, as the crossing-over rate for these loci was estimated to be less than 5 x 10-9 per base pair per generation (cf. Comeron, Kreitman, and Aguadé [1999
] and True, Mercer, and Laurie [1996] for estimated rates of crossing over).
Patterns of Synonymous and Replacement Variation
For between-species comparisons of synonymous and replacement polymorphism, I restricted the analysis to homologous loci sequenced in both species. In addition to loci referenced above, I included Adh and Adh-dup (D. simulans; Sumner 1991
), ci (Berry et al. 1991), cta (Wayne and Kreitman 1996
), Est-6 (Cooke and Oakeshott 1989
; Karotam, Delves, and Oakeshott 1993
; Hasson and Eanes 1996
), Gld (Hamblin and Aquadro 1996, 1997), janus (Kliman et al. 2000
; F. Depaulis, personal communication), Mlc1 (Leicht et al. 1995
), Pgd (Begun and Aquadro 1994
; Begun and Whitley 2000
), prune (Simmons et al. 1994
), runt (Labate, Biermann, and Eanes 1999
), and white (Kirby and Stephan 1995
; Kliman et al. 2000
). For African versus non-African comparisons of synonymous and replacement polymorphism, I considered all loci with both African and non-African samples. In this part of the analysis, I included all available Adh and Adh-dup alleles for D. melanogaster.
Sampling Locations
This study combined data from many sources. For the majority of loci in D. melanogaster, African samples had a mixed sampling scheme that included one or more lines from Botswana, Kenya, Madagascar, South Africa, or Zimbabwe. Exceptions were Boss, Ref(2)P, and Rh3, for which only two West African lines were sampled. Acp29AB, Adh, eve, Pgi, and Tpi were sampled in both East and West Africa. Non-African samples were generally a mix from diverse geographic localities, with a bias toward North America. The data of Teeter et al. (2000)
had a consistent sampling scheme for all loci: African populations were composed of one South African line and one (or two) Kenyan lines, and non-African lines were drawn from a worldwide sample. Generally, samples for D. simulans included one or more lines from East Africa. G6pd, Boss, Pgi, and Rh3 were sampled in both East and West Africa; vermilion included only West Africa. Non-African samples were generally a mix from diverse geographic localities, with a bias toward North America. Additional details can be found in the original sources (see references above).
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Results and Discussion |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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A Complex History for D. melanogaster
In table 1, I compare estimates of
W in African and non-African samples for 20 X-linked loci and 59 autosomal loci. I performed a sign test on the combined data to test the null hypothesis of equal levels of diversity in African and non-African populations (table 2
). As expected (Begun and Aquadro 1993
), X-chromosome loci had reduced levels of nucleotide diversity in non-African populations relative to African populations (17:3; P = 0.001). In contrast, loci on the autosomes were about as likely to be more variable outside of Africa as within Africa (28:33; table 2 ). Thus, as anticipated from a handful of earlier studies (Clark and Wang 1997
; Tsaur, Ting, and Wu 1998
; Begun et al. 1999
; Andolfatto and Kreitman 2000
), there existed an interesting discrepancy between the patterns observed on the X chromosome and those observed on the autosomes. Patterns for the X chromosome and the autosomes were significantly different from each other (two-tailed Fisher's exact test; P = 0.017). There is no detectable difference between chromosomes 2 and 3.
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The data of Teeter et al. (2000)
present the advantage of a consistent sampling scheme, since a similar set of lines were sampled for all markers (see Materials and Methods). In addition, unlike in many earlier studies, these loci were not chosen because of prior evidence for the action of natural selection. With the analysis restricted to these loci, a significant trend toward higher nucleotide diversity within Africa was apparent for the X-linked loci (10:2; P = 0.019), while, again, no clear trend emerged for autosomal loci (23:18; P = 0.264).
Demographic events such as a bottleneck are expected to affect the whole genome similarly (i.e., they are expected to result in lower levels of variation outside Africa). While genomes with a smaller effective population size will recover faster from changes in population size (e.g., Fay and Wu 1999
), it is unclear how relevant this will be to the interpretation of X-autosome comparisons (see arguments below). The discrepancy between the X chromosome and the autosomes is therefore difficult to explain with a simple bottleneck in the history of non-African populations. In order to reconcile all the data with the bottleneck hypothesis, we would have to invoke post hoc differences between non-African and African populations of D. melanogaster.
X-Chromosome Versus Autosome Nucleotide Diversity in D. melanogaster
Table 3
summarizes mean synonymous site diversity levels in African and non-African samples for X-linked and autosomal loci in D. melanogaster and D. simulans. Comparisons of X and autosome levels of diversity were complicated by possible differences in their effective population sizes. Assuming equal sex ratios and no selection, a simple correction is to multiply X diversities by 4/3 (based on relative numbers of X chromosomes and autosomes). However, if sexual selection on males is prevalent in natural populations of Drosophila (cf. Andersson 1994
), then the ratio of effective sizes of the X chromosome and autosomes may be closer to unity (Caballero 1995
). Sex-specific life history traits (e.g., mortality rates) in the wild may further complicate the appropriate scaling of levels of variation on the X chromosome and the autosomes (B. Charlesworth, personal communication). Unfortunately, we remain virtually ignorant of the relative importance of sexual selection and sex-specific life history traits in natural populations of D. melanogaster and D. simulans. Laboratory measurements have suggested that the effective population size of females is greater than that of males (Crow and Morton 1954
). Thus, the appropriate correction for X-chromosome diversity may be less than 4/3.
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Whatever correction factor was used, an inescapable problem emerged when considering levels of nucleotide diversity in D. melanogaster (table 3 ). When X-chromosome variation levels were left uncorrected (as they appear in table 3 ), there was a trend toward lower diversity on the non-African X chromosome relative to non-African autosomes (
W ratio = 0.7) and somewhat elevated diversity on the African X chromosome relative to African autosomes (W ratio = 1.6). If, instead, X-chromosome diversities were multiplied by 4/3, levels of variation were comparable on all chromosomes but the African X; variation on the African X chromosome was twice that of African autosomes. To establish statistical significance for these trends will require data from consistently sampled populations. In summary, the chromosome-specific differences between African and non-African populations of D. melanogaster (tables 2 and 3 ) make a simple demographic explanation, such as a bottleneck, improbable. Additional factors must be invoked to explain the discordant geographic patterns for the X chromosome versus the autosomes. Regardless of whether or not a bottleneck occurred in the history of non-African populations, we are left to explain why X-chromosome diversity appears to be elevated above that of autosomes in African populations.
A Role for Autosomal Inversions?
A possible explanation for the unexpectedly low levels of diversity for African D. melanogaster autosomes is the presence of common autosomal inversion polymorphisms. Based on the geographic distribution of inversions in this species (Lemeunier and Aulard 1992
), it is likely that autosomal inversions are more often present in our African samples than in non-African samples. Inversions suppress crossing over within the inverted region when heterozygous. Linked neutral diversity on autosomes polymorphic for inversions may therefore be more susceptible to variation-reducing selection (and thus harbor reduced variability) than are X-linked loci (cf. Begun 1996
). This explanation probably requires the persistence of inversions at appreciable frequencies. Even if this scenario explains the reduced variability on African autosomes, careful timing of inversion and bottleneck effects would be required to explain why a bottleneck pattern was not apparent in the autosomal data. Recent studies of two common inversions have suggested that they are not old and have had low historical frequencies (Wesley and Eanes 1994
; Andolfatto, Wall, and Kreitman 1999
). Thus, an alternative explanation is a recent change in inversion frequencies in Africa. This hypothesis predicts that nucleotide diversity of inverted chromosomes will be less than that of standard chromosomes (cf. Navarro, Barbadilla, and Ruiz 2000
). However, direct comparisons of inverted and standard chromosomes (Hasson and Eanes 1996
; Aguadé 1998, 1999
; Andolfatto, Wall, and Kreitman 1999
; Benassi et al. 1999
; Depaulis, Brazier, and Veuille 1999
) do not suggest markedly reduced levels of variation in inverted chromosomes (with the exception of loci very close to inversion breakpoints).
The impact of inversions in African populations can be assessed indirectly by comparing D. melanogaster/D. simulans ratios of nucleotide diversities for the X chromosome and the autosomes. Inversions are rare in D. simulans (Lemeunier and Aulard 1992
), so this species should not show the same pattern if inversions account for the reduced autosomal diversity in African D. melanogaster samples. The African D. melanogaster/D. simulans ratios of W were 0.9 for the X chromosome and 0.5 for the autosomes (table 3 ); non-African populations had more equal ratios (0.5 and 0.6, respectively). These ratios and the estimates of mean diversities on which they were based had large standard errors. In addition, we must assume that no other factors affect X-linked and autosomal variation in D. simulans. This said, the pattern was consistent with the hypothesis that inversions have decreased diversity levels on the autosomes in African populations of D. melanogaster.
Evidence for a Bottleneck in the History of D. simulans
As shown in table 1
, there are few data for D. simulans for which African/non-African comparisons of single-nucleotide polymorphisms can be made. Combining all chromosomes, a sign test (table 2
) revealed significantly lower diversity in non-African populations relative to African populations (11:2; P = 0.013). While this finding is consistent with the microsatellite survey of Irvin et al. (1998)
, a caveat in making African/non-African comparisons is the possibility of African/non-African differences in population structure. The diversity measure W is sensitive to the degree of population subdivision. In particular, when populations are subdivided and both demes are sampled, W will be larger than predicted for a panmictic population of the same total size (Tajima 1989a
). Recent data from the G6pd locus (Hamblin and Veuille 1999
) are consistent with considerable population differentiation within Africa. As an illustration, total variability at the G6pd locus in Africa is about twofold higher than total non-African diversity (table 1
). A measure which is less sensitive to population subdivision than total diversity is the average of within-population diversities (Tajima 1989a
). When average within-population diversities at G6pd were compared, African populations (W within = 0.0033 per site) were more similar to non-African populations (W within = 0.0036 per site). Similarly, the vermilion locus showed considerable between-populations differentiation within Africa (Hamblin and Veuille 1999
). In summary, while the available data for D. simulans show a trend toward higher levels of total nucleotide diversity in Africa than outside of Africa (tables 1–3 ), within-population diversities are not necessarily higher in Africa. Thus, it remains unclear whether the nucleotide data support a simple bottleneck model.
Patterns of Synonymous and Replacement Polymorphism
Table 4
lists the numbers of synonymous and replacement polymorphisms and their ratios (S/R) in D. melanogaster and D. simulans for all available pairs of homologous loci. The S/R ratio for the autosomes of D. melanogaster was significantly lower than that for D. simulans autosomes (two-tailed Fisher's exact test; P = 0.01). In contrast, S/R ratios were surprisingly similar in the two species for the X chromosome (two-tailed Fisher's exact test; P = 1.00). These findings are consistent with the X-autosome contrast first noted by Begun (1996)
. There appears to be an excess of replacement polymorphisms and/or a deficiency of synonymous polymorphisms on D. melanogaster autosomes relative to D. simulans autosomes. Also of interest is the pattern of within-species variability (table 4
). In populations of D. melanogaster, the within-species S/R ratios on the X chromosome were higher than those of the autosomes. This trend was somewhat less marked in D. simulans. Since nonhomologous loci were compared, little can be said with certainty in X-autosome comparisons. A Fisher's exact test was performed on S/R ratios under the assumption that the mean numbers of synonymous and replacement sites do not differ between the X-linked and autosomal loci. This test revealed a significantly smaller S/R ratio on autosomes relative to the X chromosome in both species (two-tailed P < 10-6 and P < 0.003 for D. melanogaster and D. simulans, respectively).
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Three genes account for most of the replacement variation on D. simulans autosomes in table 4 : anon1A3, anon1E9, and anon1G5. Since these genes were chosen for study specifically because they showed high rates of amino acid divergence between species (Schmid et al. 1999
), they may not be representative of the "average" gene in the genome. Synonymous and replacement sites of the anon genes may experience similarly weak selection intensities. When these loci were excluded from the analyses, the conclusions changed in two ways. First, the within-species X-autosome S/R difference in D. simulans disappeared. Second, the between-species autosome difference in S/R ratios became much more significant (two-tailed Fisher's exact test; P = 2 x 10-6). While there is no a priori reason to exclude the anon1A3, anon1E9, and anon1G5 genes from these comparisons, more confidence should be placed on the between-species X-autosome S/R difference than the within–D. simulans X-autosome S/R difference. The sensitivity of the results to the inclusion of the anon genes indicates that it may not be entirely appropriate to treat replacement and synonymous sites as discrete selected classes.
Models of Synonymous and Replacement Site Evolution
How can the above patterns of synonymous and replacement polymorphism be explained? One possibility is that the majority of amino acid replacement changes are deleterious and partially recessive (McVean and Charlesworth 1999
). Allow, for the moment, the three following assumptions: (1) sites evolve independently, (2) most amino acid replacement mutations are deleterious and partially recessive, and (3) selection is stronger in D. simulans than in D. melanogaster (proportional to Nes, where Ne is the effective population size and s is the mean deleterious selection coefficient). This last assumption is supported by patterns of polymorphism and divergence in these two species (Akashi 1995, 1996
). Figure 1
is a schematic diagram based on figures 2 and 4 of McVean and Charlesworth (1999)
. The key feature is that the slope of the line relating diversity to the strength of selection is less steep on autosomes than on the X chromosome due to the recessiveness of deleterious mutations. This model neatly accounts for three features of the synonymous and replacement polymorphism data: (1) the within-species S/R ratio is greater on the X chromosome than on the autosomes; (2) the X-autosome S/R discrepancy is more marked in D. melanogaster than in D. simulans; and (3) as first noted by Begun (1996)
, the D. melanogaster and D. simulans S/R ratios are more discrepant on the autosomes than on the X chromosome.
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A possible problem with the above model is that sites are assumed to evolve independently. An alternative explanation for the patterns of synonymous and replacement polymorphisms between species was offered by Begun (1996)
, who noted that transient selection on amino acid variants (cf. Gillespie 1991
) may maintain amino acid variants in natural populations and cause the reduction of linked synonymous site variation. Drosophila melanogaster autosomes generally experience lower rates of recombination than do autosomes in D. simulans due to the greater extent of centromeric and telomeric suppression of crossing over (Sturtevant 1929
). As a result, D. melanogaster autosomes should be more affected by variation-reducing selection than are those of its sister species. Transient selection on amino acid variants may also contribute to X-autosome differences within D. melanogaster if autosomal inversion polymorphisms reduce recombination on autosomes relative to the X chromosome. A proper evaluation of this model awaits quantification. Both D. melanogaster and D. simulans are thought to have recently colonized Europe and the Americas. Thus, possible targets for recent transient or geographically localized selection are loci involved in adaptation to temperate habitats. If transient selection is shaping patterns of variability at a large number of loci, we may expect S/R ratios to be lower outside of than within Africa. As seen in table 5 , S/R ratios in African and non-African populations are remarkably similar. The trend on the X toward a lower S/R ratio in non-African D. simulans is not significant (two-tailed Fisher's exact test; P = 0.347). Note that this test may lack power, since African and non-African samples share part of their genealogical histories. Nonetheless, it appears that the relatively recent range expansion from Africa, possibly accompanied by changes in effective population size, selection pressures, and changes in inversion frequencies in D. melanogaster, has not had a large effect on the dynamics of synonymous and replacement polymorphism in these two species.
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Conclusions |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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Geographic patterns of nucleotide diversity in D. melanogaster are incompatible with a simple "out of Africa" bottleneck in the history of this species. In particular, the X chromosome and autosomes show distinct patterns of geographic differentiation. If a bottleneck explains the X-chromosome pattern (i.e., higher diversity in Africa than outside of Africa), a second factor is needed to explain two observations: (1) this bottleneck pattern is not observed on the autosomes and (2) diversity levels on the African autosomes are reduced relative to African X chromosomes. A possible explanation is the presence of autosomal inversions, which are generally more numerous and occur at higher frequencies in African populations. However, a quantitative assessment of the impact of inversions on autosomal diversity levels awaits more data. The pattern in D. simulans, although suggestive of a simple bottleneck in the history of non-African populations, could also result from ancient (i.e., African) population structure.
Drosophila melanogaster autosomes harbor an excess of amino acid replacement polymorphisms (and/or a deficiency of synonymous polymorphisms) relative to D. simulans autosomes, while the X chromosome shows no such pattern. Here, I have argued that several features of within- and between-species patterns of synonymous and replacement polymorphism might be explained by assuming that replacement polymorphisms are deleterious and partially recessive and that purifying selection is more efficient in D. simulans than in D. melanogaster. Generally lower recombination rates on D. melanogaster autosomes may also contribute to this pattern if transient selection on amino acid variants is common.
This study highlights problems encountered in comparisons of X-linked and autosomal loci. Many factors, both selective and demographic, can contribute to sex-autosome differences in levels of nucleotide diversity (Aquadro, Begun, and Kindahl 1994
; Caballero 1995
; Charlesworth 1996
; Fay and Wu 1999
). It has been proposed that X-autosome comparisons may provide a way to distinguish between background selection and positive selection in the genome (Aquadro, Begun, and Kindahl 1994
). For example, if most advantageous alleles are recessive, hitchhiking models (Maynard-Smith and Haigh 1974
) predict reduced diversity on the X chromosome relative to autosomes, whereas the background selection hypothesis (Charlesworth, Morgan, and Charlesworth 1993
) predicts the opposite pattern (Aquadro, Begun, and Kindahl 1994
). Thus, adaptation to temperate habitats may explain the larger diversity reductions on the X chromosome relative to autosomes in non-African populations of both D. melanogaster and D. simulans (tables 1–3
; see also Begun and Whitley 2000
). However, we still have a poor understanding of how ancient population structure and recent demographic perturbations may have affected levels of nucleotide variation (in addition to the unknown impact of inversion polymorphisms in D. melanogaster). Comparisons of X and autosome nucleotide diversities may not be informative about the mode of selection as long as a panmictic population model remains the null hypothesis.
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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F. Depaulis, G. Gibson, R. Kulathinal, R. Kliman, C. Langley, K. Schmid, and S. C. Tsaur kindly provided data prior to its publication. Thanks to D. Bachtrog, B. Charlesworth, I. Gordo, G. McVean, A. Navarro, D. Rand, two anonymous reviewers, and especially M. Przeworski for helpful discussions and comments on the manuscript. P.A. was supported by an EMBO postdoctoral fellowship.
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Footnotes |
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David M. Rand, Reviewing Editor
1 Keywords: bottleneck
selection
deleterious mutations
polymorphism
inversion
synonymous
nonsynonymous
dominance 
2 Address for correspondence and reprints: Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom. peter.andolfatto{at}ed.ac.uk
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literature cited |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsliterature cited |
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Aguadé, M. 1998. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. Genetics 150:1079–1089.
———. 1999. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics 152:543–51.
Akashi, H. 1995. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139:1067–1076.
———. 1996. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144:1297–1307.
Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, N.J.
Andolfatto, P., and M. Kreitman. 2000. Molecular variation at the In(2L)t proximal breakpoint site in natural populations of Drosophila melanogaster and D. simulans. Genetics 154:1681–1691.
Andolfatto, P., J. D. Wall, and M. Kreitman. 1999. Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics 153:1297–1311.
Aquadro, C. F., D. J. Begun, and E. C. Kindahl. 1994. Selection, recombination, and DNA polymorphism in Drosophila. Pp. 46–56 in B. Golding, ed. Non-neutral evolution: theories and molecular data. Chapman and Hall, New York.
Ayala, F. J., B. S. Chang, and D. L. Hartl. 1993. Molecular evolution of the Rh3 gene in Drosophila. Genetica 92:23–32.
Ayala, F. J., and D. L. Hartl. 1993. Molecular drift of the Bride of Sevenless (boss) gene in Drosophila. Mol. Biol. Evol. 10:1030–1040.[Abstract]
Begun, D. J. 1996. Population genetics of silent and replacement variation in Drosophila simulans and D. melanogaster: X/autosome differences? Mol. Biol. Evol. 13:1405–1407.[Web of Science][Medline]
Begun, D. J., and C. F. Aquadro. 1993. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365:548–550.
———. 1994. Evolutionary inferences from DNA variation at the 6-Phosphogluconate Dehydrogenase locus in natural populations of Drosophila—selection and geographic differentiation. Genetics 136:155–171.
———. 1995. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics 140:1019–1032.
Begun, D. J., A. J. Betancourt, C. H. Langley, and W. Stephan. 1999. Is the fast/slow allozyme variation at the Adh locus of Drosophila melanogaster an ancient balanced polymorphism? Mol. Biol. Evol. 16:1816–1819.[Web of Science][Medline]
Begun, D. J., and P. Whitley. 2000. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc. Natl. Acad. Sci. USA 97:5960–5965.
Benassi, V., F. Depaulis, G. K. Meghlaoui, and M. Veuille. 1999. Partial sweeping of variation at the Fbp2 locus in a west African population of Drosophila melanogaster. Mol. Biol. Evol. 16:347–353.[Abstract]
Berry, A. J., J. W. Ajioka, and M. Kreitman. 1991. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129:1111–1117.
Caballero, A. 1995. On the effective size of populations with separate sexes, with particular reference to sex-linked genes. Genetics 139:1007–1011.
Charlesworth, B. 1996. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet. Res. 68:131–149.
Charlesworth, B., M. T. Morgan, and D. Charlesworth. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303.
Clark, A. G., and L. Wang. 1997. Molecular population genetics of Drosophila immune system genes. Genetics 147:713–724.
Comeron, J. M., M. Kreitman, and M. Aguadé. 1999. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151:239–249.
Cooke, P. H., and J. G. Oakeshott. 1989. Amino acid polymorphisms for Esterase 6 in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 86:1426–1430.
Crow, J., and N. E. Morton. 1954. Measurement of gene frequency drift in small populations. Evolution 9:202–214.
David, J. R., and P. Capy. 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4:106–111.[Web of Science][Medline]
Depaulis, F., L. Brazier, and M. Veuille. 1999. Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism. Genetics 152:1017–1024.
Eanes, W. F., M. Kirchner, J. Yoon, C. H. Biermann, I. N. Wang, M. A. McCartney, and B. C. Verrelli. 1996. Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics 144:1027–1041.
Fay, J. C., and C. I. Wu. 1999. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol. Biol. Evol. 16:1003–1005.[Web of Science][Medline]
Gasperini, R., and G. Gibson. 1999. Absence of protein polymorphism in the Ras genes of Drosophila melanogaster. J. Mol. Evol. 49:583–590.[Medline]
Gillespie, J. H. 1991. The causes of molecular evolution. Oxford University Press, Oxford, England.
Hale, L. R., and R. S. Singh. 1991. A comprehensive study of genic variation in natural populations of Drosophila melanogaster. IV. Mitochondrial DNA variation and the role of history vs. selection in the genetic structure of geographic populations. Genetics 129:103–117.
Hamblin, M. T., and C. F. Aquadro. 1996. High nucleotide sequence variation in a region of low recombination in Drosophila simulans in consistent with background selection. Mol. Biol. Evol. 13:1133–1140.[Abstract]
———. 1997. Contrasting patterns of nucleotide sequence variation at the glucose dehydrogenase (Gld) locus in different populations of Drosophila melanogaster. Genetics 145:1053–1062.
Hamblin, M. T., and M. Veuille. 1999. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics 153:305–317.
Hasson, E., and W. F. Eanes. 1996. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics 144:1565–1575.
Hasson, E., I. N. Wang, L. W. Zeng, M. Kreitman, and W. Eanes.1998 . Nucleotide variation in the Triose Phosphate Isomerase (Tpi) locus of Drosophila melanogaster and D. simulans. Mol. Biol. Evol. 15:756–769.[Abstract]
Hey, J., and R. M. Kliman. 1993. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol. Biol. Evol. 10:804–822.[Abstract]
Hilton, H., R. M. Kliman, and J. Hey. 1994. Using hitchhiking genes to study adaptation and divergence during speciation within the Drosophila melanogaster complex. Evolution 48:1900–1913.
Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164.
Inomata, N., H. Shibata, E. Okuyama, and T. Yamazaki. 1995. Evolutionary relationships and sequence variation of alpha-Amylase variants encoded by duplicated genes in the Amy locus of Drosophila melanogaster. Genetics 141:237–244.
Irvin, S. D., K. A. Wetterstrand, C. M. Hutter, and C. F. Aquadro. 1998. Genetic variation and differentiation at microsatellite loci in Drosophila simulans. Evidence for founder effects in New World populations. Genetics 150:777–790.
Karotam, J., A. C. Delves, and J. G. Oakeshott. 1993. Conservation and change in structural and 5' flanking sequences of esterase 6 in sibling Drosophila species. Genetica 88:11–28.
Kirby, D. A., and W. Stephan. 1995. Haplotype test reveals departure from neutrality in a segment of the white gene of Drosophila melanogaster. Genetics 141:1483–1490.
Kliman, R. M., P. Andolfatto, J. A. Coyne, F. Depaulis, M. Kreitman, A. J. Berry, J. McCarter, J. Wakeley, and J. Hey. 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913–1931.
Kliman, R. M., and J. Hey. 1993. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics 133:375–387.
Kreitman, M., and R. Hudson. 1991. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127:565–582.
Labate, J. A., C. H. Biermann, and W. F. Eanes. 1999. Nucleotide variation at the runt locus in Drosophila melanogaster and D. simulans. Mol. Biol. Evol. 16:724–731.[Abstract]
Lachaise, D., L. M. Cariou, J. R. David, F. Lemeunier, L. Tsacas, and M. Ashburner. 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22:159–225.
Langley, C. H., B. P. Lazzaro, W. Philips, E. Heikinen, and J. Braverman. 2000. Linkage disequilibria and the site frequency spectra in the su(s) and su(wa) regions of the Drosophila melanogaster X chromosome. Genetics 156:1837–1852.
Leicht, B. G., S. V. Muse, M. Hanczyc, and A. G. Clark. 1995. Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. Genetics 139:299–308.
Lemeunier, F., and S. Aulard. 1992. Inversion polymorphism in Drosophila melanogaster. Pp. 339–405 in C. B. Krimbas and J. R. Powell, eds. Drosophila inversion polymorphism. CRC Press, Boca Raton, Fla.
Ludwig, M. Z., and M. Kreitman. 1995. Evolutionary dynamics of the enhancer regions of even-skipped in Drosophila. Mol. Biol. Evol. 12:1002–1011.[Abstract]
McVean, G. A. T., and B. Charlesworth. 1999. A population genetic model for the evolution of synonymous codon usage: patterns and predictions. Genet. Res. 74:145–158.
Maynard Smith, J., and J. Haigh. 1974. The hitch-hiking effect of a favourable gene. Genet. Res. 23:23–35.[Web of Science][Medline]
Moriyama, E. N., and J. R. Powell. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol. Biol. Evol. 13:261–277.[Abstract]
Navarro, A., A. Barbadilla, and A. Ruiz. 2000. Effect of inversion polymorphism on the nucleotide variability of linked chromosomal regions. Genetics 155:685–698.
Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175.
Schlötterer, C., C. Vogl, and D. Tautz. 1997. Polymorphism and locus-specific effects on polymorphism at microsatellite loci in natural Drosophila melanogaster populations. Genetics 146:309–320.
Schmid, K. J., L. Nigro, C. H. Aquadro, and D. Tautz. 1999. Large number of replacement polymorphisms in rapidly evolving genes of Drosophila: implications for genome-wide surveys of DNA polymorphism. Genetics 153:1717–1729.
Simmons, G. M., W. Kwok, P. Matulonis, and T. Venkatesh. 1994. Polymorphism and divergence at the prune locus in Drosophila melanogaster and D. simulans. Mol. Biol. Evol. 11:666–671.[Abstract]
Sokal, R. R., and F. J. Rohlf. 1998. Biometry. W. H. Freeman, New York.
Sturtevant, A. H. 1929. The genetics of Drosophila simulans. Carnegie Inst. Wash. Publ. 399:1–62.
Sumner, C. J. 1991. Nucleotide polymorphism in the Alcohol Dehydrogenase duplicate locus of Drosophila simulans: implications for the neutral theory. Undergraduate thesis, Princeton University, Princeton, N.J.
Tajima, F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460.
———. 1989a. DNA polymorphism in a subdivided population: the expected number of segregating sites in the two-subpopulation model. Genetics 123:229–240.
———. 1989b. The effect of change in population size on DNA polymorphism. Genetics 123:597–601.
Teeter, K., M. Naeemuddin, R. Gasperini, E. Zimmerman, K. P. White, R. Hoskins, and G. Gibson. 2000. Haplotype dimorphism in a SNP collection from Drosophila melanogaster. J. Exp. Zool. 288:63–75.
Tsaur, S. C., C. T. Ting, and C. I. Wu. 1998. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol. Biol. Evol. 15:1040–1046.[Abstract]
Walthour, C. S., and S. W. Schaeffer. 1994. Molecular population genetics of sex determining genes: the transformer gene of Drosophila melanogaster. Genetics 136:1367–1372.
Watterson, G. A. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7:256–276.[Web of Science][Medline]
Wayne, M. L., D. Contamine, and M. Kreitman. 1996. Molecular population genetics of Ref(2)P, a locus which confers viral resistance in Drosophila. Mol. Biol. Evol. 13:191–199.[Abstract]
Wayne, M. L., and M. Kreitman. 1996. Reduced variation at concertina, a heterochromatic locus in Drosophila. Genet. Res. 68:101–108.[Medline]
Wesley, C. S., and W. F. Eanes. 1994. Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 91:3132–3136.
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|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
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J. F. Storz, B. A. Payseur, and M. W. Nachman Genome Scans of DNA Variability in Humans Reveal Evidence for Selective Sweeps Outside of Africa Mol. Biol. Evol., September 1, 2004; 21(9): 1800 - 1811. [Abstract] [Full Text] [PDF]
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D. J. Orengo and M. Aguade Detecting the Footprint of Positive Selection in a European Population of Drosophila melanogaster: Multilocus Pattern of Variation and Distance to Coding Regions Genetics, August 1, 2004; 167(4): 1759 - 1766. [Abstract] [Full Text] [PDF]
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E. Baudry, B. Viginier, and M. Veuille Non-African Populations of Drosophila melanogaster Have a Unique Origin Mol. Biol. Evol., August 1, 2004; 21(8): 1482 - 1491. [Abstract] [Full Text] [PDF]
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G. Schofl and C. Schlotterer Patterns of Microsatellite Variability Among X Chromosomes and Autosomes Indicate a High Frequency of Beneficial Mutations in Non-African D. simulans Mol. Biol. Evol., July 1, 2004; 21(7): 1384 - 1390. [Abstract] [Full Text] [PDF]
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V. B. DuMont, J. C. Fay, P. P. Calabrese, and C. F. Aquadro DNA Variability and Divergence at the Notch Locus in Drosophila melanogaster and D. simulans: A Case of Accelerated Synonymous Site Divergence Genetics, May 1, 2004; 167(1): 171 - 185. [Abstract] [Full Text] [PDF]
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W. Wang, K. Thornton, J. J. Emerson, and M. Long Nucleotide Variation and Recombination Along the Fourth Chromosome in Drosophila simulans Genetics, April 1, 2004; 166(4): 1783 - 1794. [Abstract] [Full Text] [PDF]
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J. W. O. Ballard Sequential Evolution of a Symbiont Inferred From the Host: Wolbachia and Drosophila simulans Mol. Biol. Evol., March 1, 2004; 21(3): 428 - 442. [Abstract] [Full Text] [PDF]
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D. L. Halligan, A. Eyre-Walker, P. Andolfatto, and P. D. Keightley Patterns of Evolutionary Constraints in Intronic and Intergenic DNA of Drosophila Genome Res., February 1, 2004; 14(2): 273 - 279. [Abstract] [Full Text] [PDF]
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E. Gravot, M. Huet, and M. Veuille Effect of Breeding Structure on Population Genetic Parameters in Drosophila Genetics, February 1, 2004; 166(2): 779 - 788. [Abstract] [Full Text] [PDF]
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M. H. Kohn, S. Fang, and C.-I Wu Inference of Positive and Negative Selection on the 5' Regulatory Regions of Drosophila Genes Mol. Biol. Evol., February 1, 2004; 21(2): 374 - 383. [Abstract] [Full Text] [PDF]
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R. Piccinali, M. Aguade, and E. Hasson Comparative Molecular Population Genetics of the Xdh Locus in the Cactophilic Sibling Species Drosophila buzzatii and D. koepferae Mol. Biol. Evol., January 1, 2004; 21(1): 141 - 152. [Abstract] [Full Text] [PDF]
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E. S. Balakirev and F. J. Ayala Nucleotide Variation of the Est-6 Gene Region in Natural Populations of Drosophila melanogaster Genetics, December 1, 2003; 165(4): 1901 - 1914. [Abstract] [Full Text] [PDF]
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M. D. Dean, K. J. Ballard, A. Glass, and J. W. O. Ballard Influence of Two Wolbachia Strains on Population Structure of East African Drosophila simulans Genetics, December 1, 2003; 165(4): 1959 - 1969. [Abstract] [Full Text] [PDF]
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M. O. Kauer, D. Dieringer, and C. Schlotterer A Microsatellite Variability Screen for Positive Selection Associated With the "Out of Africa" Habitat Expansion of Drosophila melanogaster Genetics, November 1, 2003; 165(3): 1137 - 1148. [Abstract] [Full Text] [PDF]
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L. A. Sheldahl, D. M. Weinreich, and D. M. Rand Recombination, Dominance and Selection on Amino Acid Polymorphism in the Drosophila Genome: Contrasting Patterns on the X and Fourth Chromosomes Genetics, November 1, 2003; 165(3): 1195 - 1208. [Abstract] [Full Text] [PDF]
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D. Bachtrog Protein Evolution and Codon Usage Bias on the Neo-Sex Chromosomes of Drosophila miranda Genetics, November 1, 2003; 165(3): 1221 - 1232. [Abstract] [Full Text] [PDF]
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S. Glinka, L. Ometto, S. Mousset, W. Stephan, and D. De Lorenzo Demography and Natural Selection Have Shaped Genetic Variation in Drosophila melanogaster: A Multi-locus Approach Genetics, November 1, 2003; 165(3): 1269 - 1278. [Abstract] [Full Text] [PDF]
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P. Andolfatto and J. D. Wall Linkage Disequilibrium Patterns Across a Recombination Gradient in African Drosophila melanogaster Genetics, November 1, 2003; 165(3): 1289 - 1305. [Abstract] [Full Text] [PDF]
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S. Yi, D. Bachtrog, and B. Charlesworth A Survey of Chromosomal and Nucleotide Sequence Variation in Drosophila miranda Genetics, August 1, 2003; 164(4): 1369 - 1381. [Abstract] [Full Text] [PDF]
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T. A. Schlenke and D. J. Begun Natural Selection Drives Drosophila Immune System Evolution Genetics, August 1, 2003; 164(4): 1471 - 1480. [Abstract] [Full Text] [PDF]
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M. Przeworski Estimating the Time Since the Fixation of a Beneficial Allele Genetics, August 1, 2003; 164(4): 1667 - 1676. [Abstract] [Full Text] [PDF]
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X. Maside, C. Bartolome, and B. Charlesworth Inferences on the Evolutionary History of the S-Element Family of Drosophila melanogaster Mol. Biol. Evol., August 1, 2003; 20(8): 1183 - 1187. [Abstract] [Full Text] [PDF]
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M. Kauer, D. Dieringer, and C. Schlotterer Nonneutral Admixture of Immigrant Genotypes in African Drosophila melanogaster Populations from Zimbabwe Mol. Biol. Evol., August 1, 2003; 20(8): 1329 - 1337. [Abstract] [Full Text] [PDF]
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D. J. Begun and P. Whitley Molecular Population Genetics of Xdh and the Evolution of Base Composition in Drosophila Genetics, December 1, 2002; 162(4): 1725 - 1735. [Abstract] [Full Text] [PDF]
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A. Eyre-Walker Changing Effective Population Size and the McDonald-Kreitman Test Genetics, December 1, 2002; 162(4): 2017 - 2024. [Abstract] [Full Text] [PDF]
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A. Eyre-Walker, P. D. Keightley, N. G. C. Smith, and D. Gaffney Quantifying the Slightly Deleterious Mutation Model of Molecular Evolution Mol. Biol. Evol., December 1, 2002; 19(12): 2142 - 2149. [Abstract] [Full Text] [PDF]
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R. A. Holt, G. M. Subramanian, A. Halpern, G. G. Sutton, R. Charlab, D. R. Nusskern, P. Wincker, A. G. Clark, J. M. C. Ribeiro, R. Wides, et al. The Genome Sequence of the Malaria Mosquito Anopheles gambiae Science, October 4, 2002; 298(5591): 129 - 149. [Abstract] [Full Text] [PDF]
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W. A. Odgers, C. F. Aquadro, C. W. Coppin, M. J. Healy, and J. G. Oakeshott Nucleotide Polymorphism in the Est6 Promoter, Which Is Widespread in Derived Populations of Drosophila melanogaster, Changes the Level of Esterase 6 Expressed in the Male Ejaculatory Duct Genetics, October 1, 2002; 162(2): 785 - 797. [Abstract] [Full Text] [PDF]
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A. J. Betancourt, D. C. Presgraves, and W. J. Swanson A Test for Faster X Evolution in Drosophila Mol. Biol. Evol., October 1, 2002; 19(10): 1816 - 1819. [Full Text] [PDF]
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J. D. Wall, P. Andolfatto, and M. Przeworski Testing Models of Selection and Demography in Drosophila simulans Genetics, September 1, 2002; 162(1): 203 - 216. [Abstract] [Full Text] [PDF]
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G. Marais and G. Piganeau Hill-Robertson Interference is a Minor Determinant of Variations in Codon Bias Across Drosophila melanogaster and Caenorhabditis elegans Genomes Mol. Biol. Evol., September 1, 2002; 19(9): 1399 - 1406. [Abstract] [Full Text] [PDF]
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K. Thornton and M. Long Rapid Divergence of Gene Duplicates on the Drosophila melanogaster X Chromosome Mol. Biol. Evol., June 1, 2002; 19(6): 918 - 925. [Abstract] [Full Text] [PDF]
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M. A. Jensen, B. Charlesworth, and M. Kreitman Patterns of Genetic Variation at a Chromosome 4 Locus of Drosophila melanogaster and D. simulans Genetics, February 1, 2002; 160(2): 493 - 507. [Abstract] [Full Text] [PDF]
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M. Kauer, B. Zangerl, D. Dieringer, and C. Schlotterer Chromosomal Patterns of Microsatellite Variability Contrast Sharply in African and Non-African Populations of Drosophila melanogaster Genetics, January 1, 2002; 160(1): 247 - 256. [Abstract] [Full Text] [PDF]
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P. Andolfatto and M. Przeworski Regions of Lower Crossing Over Harbor More Rare Variants in African Populations of Drosophila melanogaster Genetics, June 1, 2001; 158(2): 657 - 665. [Abstract] [Full Text] [PDF]
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