Institut für Tierzucht und Genetik, Vienna, Austria
Correspondence: E-mail: christian.schloetterer{at}vu-wien.ac.at.
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Abstract |
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Key Words: Drosophila melanogaster gene flow selection habitat adaptation antagonistic pleiotropy
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Introduction |
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Material and Methods |
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Fly Strains
Zimbabwe flies were sampled from two locations, Sengwa Wildlife Reserve (ZS) or the capital city of Zimbabwe, Harare (ZH), and were kindly provided by C. F. Aquadro and C.-I. Wu. The lines established from both populations were propagated in the same laboratories, making them equally exposed to possible contamination by other D. melanogaster lines. To account for inbreeding effects in the Zimbabwean isofemale lines, we randomly discarded one allele from heterozygous individuals. European flies were from Italy (Naples and Rome, collected 1998 and 2001), Poland (Katovice, collected by Jacek Gorczyca, 2000) and Germany (Friedrichshafen, collected by B. Harr, 1998). Naples and Katovice flies were typed for the third chromosome; Rome and Friedrichshafen flies were typed for the X chromosome. For each European population, 30 F1 individuals (i.e., first generation progeny from a single, wild-caught, inseminated female) were used. Note that the fact that different populations are used for different chromosomes had purely technical reasons and does not introduce a bias as genetic differentiation between European populations is very low among the analyzed populations (table 1).
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Interpretation of X Chromosomal and Third Chromosomal Differences
In this study, we performed a comparison of X chromosomes and autosomes. This may be complicated because these chromosomes differ for features like levels of variability (Andolfatto 2001; Kauer et al. 2002) and the presence of inversions (Lemeunier and Aulard 1992). Inversions can reduce the recombination rate on the autosomes, which in turn affects levels of natural variability (Begun and Aquadro 1992). In our study, however, we analyzed two African populations, which were similar in their X chromosomal (Harare: H = 0.77; Sengwa: H = 0.76) and autosomal (Harare: H = 0.66; Sengwa: H = 0.61) levels of variability and also in their allele distribution. Hence, all the above mentioned differences are expected to apply to both African populations to the same extent. Patterns differing between these populations are therefore unlikely to be caused by these features.
Bayesian Admixture Analysis
The program Structure (Pritchard, Stephens, and Donnelly 2000) was used to assign individuals to homogenous clusters (populations) without consideration of the sampling localities. This program uses a Bayesian modelbased clustering method for multilocus genotypes to simultaneously determine the most probable number of homogenous populations in a given data set and assign individuals to one or more of them. The number of clusters is inferred by calculating the probability P(X|K) of the data given a certain prior value of K (number of clusters) over a number of Monte Carlo Markov Chain (MCMC) iterations. The posterior probabilities P(K|X) can be calculated following Bayes' rule. The clusters are characterized by different allele frequencies, and, according to their allele distributions, individuals are probabilistically assigned to one or more clusters. The scores of individuals in the clusters correspond to the probability of ancestry in any one of them. In this study we assumed prior values of K from 1 to 5. All calculations shown in this report are based on 1,000,000 iterations of the MCMC, after a "burn-in" period of 50,000 iterations. (The burn-in period are the first iterations of the MCMC, which are dependent on the start configuration. These iterations are not incorporated in the final calculation of the posterior probability [Pritchard, Stephens, and Donnelly 2000].) We ran the program without incorporation of prior population information. Before extracting definite values, we ran the program for each prior of K for different numbers of iterations to check for homogeneity over runs. Long runs were made to get accurate estimations of P(X|K) (Pritchard, Stephens, and Donnelly 2000). All simulations were run under a model that allows for admixture between populations (Admixture model). We also used a new, unpublished version of Structure (version II, available from http://pritch.bsd.uchicago.edu/) to incorporate linkage information between the markers and to use a different model that accounts for correlation of allele frequencies among populations due to shared history (D. Falush et al., personal communication; see also description of the program available at the above internet site). Genetic map distances for D. melanogaster were downloaded from http://flybase.bio.indiana.edu/maps/lk/cytotable.txt. If not stated otherwise, we used the old version of Structure.
To check for heterogeneity of admixture along the chromosome, we divided our data for both chromosomes into five blocks of 14 to 18 adjacent microsatellites. On the third chromosome, we discarded two loci for this analysis that were not close to any other microsatellites. The absolute nucleotide positions (Mb) in the Drosophila sequence (release 2, available from: http://flybase.bio.indiana.edu/) and cytological positions (polythene bands) that were covered by the locus sets X-1 to X-5 and 3-1 to 3-5 on the respective chromosomes were X chromosome, X-1: 15 loci, Mb 1.31 to 3.52, band 1E-3F; X-2: 15 loci, Mb 3.64 to 5.67, band 3F-5C; X-3: 15 loci, Mb 5.71 to 9.32, band 5C-8E; X-4: 15 loci, Mb 9.32 to 14.55, band 8E-12F; X-5: 14 loci, Mb 15.14 to 19.94, band 13C-19C; chromosome 3, 3-1: 18 loci, Mb 3L2.29 to 10.13, band 62C-67D; 3-2: 14 loci, Mb 3R0.78 to 3.25, band 82C-84D; 3-3: 14 loci, Mb 3R3.64 to 5.87, band 84d-85f; 3-4: 14 loci, Mb 3R5.88 to 16.18, band 85f-92e; 3-5: 15 loci, Mb 3R17.29 to 26.33, band 93e-100a. For each of these blocks, we ran Structure with K = 2 (all other settings as above).
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Results |
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We used a Bayesian modelbased clustering method (Pritchard, Stephens, and Donnelly 2000) to investigate the hypothesis of a different amount of European ("cosmopolitan") alleles in the two populations from Zimbabwe and among X chromosomes and third chromosomes. For both chromosomes, we obtained the highest posterior probability for two clusters (K = 2, table 3), which corresponded to African and European populations. Using the admixture model of Structure, the clustering method also estimates the probability of ancestry for each individual in one of the two groups (African-European). Whereas all European individuals had very high probabilities of ancestry in only one group ("the European cluster"), African individuals were found to score in both groups (table 4). The probabilities of ancestry of African individuals in the European cluster were ranging from 0% up to 70% (data not shown, but see Appendix A). Consistent with FST analysis, we found the probability of ancestry in the European cluster to differ sharply between the two Zimbabwean populations as well as between chromosomes (table 4). The highest scores for Zimbabwean individuals in the European cluster were found on the third chromosome in the capital Harare, whereas the rural population, Sengwa, shows significantly less influence of the cosmopolitan type (table 4) (P < 0.01, Mann-Whitney U test). For the X chromosome, on the other hand, scores in the European cluster are significantly lower than for the autosome (table 4) (P < 0.001, Mann-Whitney U test). Despite not being statistically significant, a trend for more European alleles in the Harare population can also be seen on the X chromosome (table 4). As this analysis was based on a substantially larger number of non-African chromosomes than African ones (120 versus 35 on chromosome 3 and 120 versus 26 on the X chromosome), we repeated the analysis with a data set in which a number of European chromosomes were randomly discarded so that equal numbers of chromosomes in African and European flies were compared. This reduced data set resulted in the same difference between the X chromosomes and the autosome for the Sengwa and Harare population (Appendix A). Hence, the Bayesian modelbased clustering method provided strong support for the presence of a larger number of European alleles on the third chromosome in the Harare population than expected by either X chromosomal data or the rural Sengwa population. The same qualitative differences between chromosomes and populations were observed when we used a newer version of Structure, which accounts for linkage among microsatellite loci or the shared history of African and non-African D. melanogaster populations (data not shown).
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Discussion |
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An issue of special interest are chromosomal inversions known to segregate on the autosomes of D. melanogaster at high frequencies (Lemeunier and Aulard 1992). The heterogeneity in admixture among individuals and chromosomal regions (fig. 1b and Appendix B) could, in principle, be also attributed to chromosomal inversions. For example, old inversions causing tight linkage among loci on the third chromosome that are segregating in Zimbabwe populations but are fixed in European populations (e.g., due to selection) could be misinterpreted as admixture of non-African alleles. Such a scenario, however, is unlikely to account for the inferred non-African ancestry in Zimbabwe, as Sengwa and Harare showed very low differentiation over all loci (table 1) and also locus-wise FST values did not provide evidence for differentiated genomic regions. Thus, if the inversions have been segregating in Zimbabwe for a long time they should be shared between both populations and occur at similar frequencies.
As we observed a high fraction of non-African alleles on the third chromosome only in Harare, this scenario seems to be not compatible with our data. Nevertheless, direct proof that Sengwa and Harare populations are not differentiated with respect to inversions could be only gained if these populations were karyotyped.
Alternatively, our observation could be explained by a combination of selection and demography. Whereas in the rural Sengwa population, Zimbabwean ancestry was observed for both chromosomes, non-African ancestry up to 70% was detected on the third chromosome in the Harare population. In several individuals collected in Harare, we detected chromosomal segments of almost pure non-African descent (>80% [Appendix A]). This result suggests that the rural population experiences less admixture of non-African genotypes than the population collected at the capital Harare. This is consistent with more transportation from Europe to the capital than to the wildlife reserve and also with other studies from D. melanogaster in Africa that found more "cosmopolitan-like" flies in towns than in the countryside (Vouidibio et al. 1989; Capy, Pla, and David 1993). Importantly, we also found a striking difference between the third chromosome and X chromosome in Harare. As neutral admixture affects both chromosomes to the same extent, admixture alone is not sufficient to explain our data.
In the following we discuss different nonneutral scenarios, which could potentially explain the observed pattern of admixture. First we discuss the possibility that European alleles could have a selective advantage in the Zimbabwean populations (i.e., positive selection for introgressed alleles in Zimbabwe). In contrast, the next two sections assume that European alleles have a selective disadvantage in Zimbabwe (i.e., purifying selection against these alleles in Zimbabwe).
Beneficial Effects of European Alleles
One nonneutral explanation for the different degree of admixture could be that some of the European alleles could have a selective advantage in Zimbabwe. A potential example could be insecticide resistance, which has recently been suggested to have spread throughout worldwide populations (Daborn et al. 2001). With the fixation of such beneficial alleles during a selective sweep, a larger genomic region around such alleles could be fixed in the African population via hitchhiking (Maynard Smith and Haigh 1974). Hence, if several beneficial alleles are located on the third chromosome, this would result in more admixture on the third chromosome than on the X chromosome. However, it is not obvious that multiple beneficial alleles should be located on the third chromosome, but none on the X chromosome. Whether the different environments from which the African populations were sampled (urban versus rural) affect the degree of admixture cannot be inferred from our data, as our sample sizes are rather restricted. The absence of the European alleles in the Sengwa sample might either be due to restricted gene flow between Sengwa and Harare or to selection against European alleles in the rural populations. Studying larger sample sizes and sample gradients from the town to the countryside could shed more light on this.
Sexual Selection
Sexual selection assumes that fast evolving traits for mating preferences could have evolved in different directions in the Zimbabwean and non-African populations. A secondary contact of populations divergent for mating preferences could therefore result in assortative mating and in postmating isolation. Interestingly, such a pattern of mating preference has been described for the Zimbabwean populations, the Z-M mating behavior (Wu et al. 1995; Hollocher et al. 1997a). In brief D. melanogaster from Zimbabwe (Z) and also from some other African populations prefer to mate with flies from their own populations when given the choice between these and so called "cosmopolitan flies" (M) (i.e., flies from outside of Africa). This mating difference was found to be asymmetrical in two ways. First only African flies discriminate but not non-African flies. Second only female African flies discriminate; males readily mate with cosmopolitan females. Whereas a wide range of Z-values (degree of mate discrimination of females) was observed in the Harare population, the rural Sengwa population had on average a stronger Z-like (i.e., discriminating) mating behavior (Hollocher et al. 1997a). Mapping studies indicated that the assortative mating behavior mapped primarily to the autosomes, but only small effects were found on the X chromosome (Hollocher et al. 1997b; Ting, Takahashi, and Wu 2001). More recently evidence for a postmating barrier was also found as crosses of Z-females with cosmopolitan males yielded fewer offspring than the reciprocal cross (Alipaz, Wu, and Karr 2001).
The asymmetry of the M-Z trait makes it difficult to predict to what extent the mixing of Zimbabwean and cosmopolitan populations is impaired by this behavior. For example, the preference of mating in one direction (M females with Z males) could impose a form of differential selection (e.g., stronger selection on the introgressed X chromosome in males [see below]) on the introgression of X chromosomes versus autosomes. On the other hand, less admixture could be expected on the third chromosome because most variance for the mating trait has been mapped to the autosomes (Hollocher et al. 1997b; Ting, Takahashi, and Wu 2001). To confirm that the higher admixture is a general phenomenon of autosomes, rather than of the third chromosome, we reanalyzed a new data set consisting of microsatellite variation on the X chromosome and the second chromosome (Caracristi and Schlötterer 2003) in Zimbabwe/Harare and non-African populations. Despite that a smaller number of loci was characterized, we also found less admixture in Harare on the X chromosome than on the second chromosome in the data set of Caracristi and Schlötterer (2003) (data not shown). The low degree of admixture on the X chromosome seems to contrast the observation that most of the genes involved in Z-ness are located on the autosomes. Nevertheless, it has to be noted that QTL maps, such as the one constructed by Hollocher et al. (1997b), are not expected to reflect the different selection intensities on X chromosomes and autosomes under natural conditions.
Ecological Selection
As a consequence of adaptation to one habitat fitness can be reduced in another habitat, leading to a reduction in gene flow between populations adapted to two different habitats (Cooper and Lenski 2000; Hawthorne and Via 2001; Hendry 2001). Both theoretical and experimental studies demonstrated that such an ecological adaptation mediated reduction in gene flow could even result in speciation (Rice and Hostert 1993; Gavrilets 1999; Schluter 2001; Ogden and Thorpe 2002). Examples could be thermal adaptation or changes in life cycle to adapt to temperate climates. Based on the population history of D. melanogaster it has previously been suggested that the habitat expansion out of Africa was facilitated by selective sweeps (Begun and Aquadro 1995; Kirby and Stephan 1996; Kauer et al. 2002). Recently, various studies have provided independent evidence that the fixation of beneficial mutations is more common than assumed under the neutral theory of molecular evolution (Kimura 1983; Bustamante et al. 2002; Fay, Wyckoff, and Wu 2002; Smith and Eyre-Walker 2002). Furthermore, adaptive explanations were also suggested for phenotypic traits differing between African and non-African populations (Vouidibio et al. 1989; Takahashi et al. 2001). If non-African flies have accumulated many mutations enhancing fitness outside of Africa, they can be expected to have lost some of their adaptations to the African environment. Such ecological trade-offs ("antagonistic pleiotropy") were demonstrated in experimental E. coli populations (Cooper and Lenski 2000; Cooper, Bennett and Lenski 2001). European alleles could, therefore, be deleterious in an African context and should be purged from the population by natural selection. Our results also have similarity to other studies, which described strong selection against hybrids and thus a maintenance of the integrity of divergent populations (Via, Bouck, and Skillman 2000; Hawthorne and Via 2001). However we have no direct evidence for antagonistic pleiotropy of differential adapted alleles in and outside of Africa. Therefore, it remains speculative whether our results could be explained by environmental selection.
Stronger Selection on the X Chromosome
The observed difference between X chromosomes and autosomes could be caused by hemizygosity of the X chromosomes in males. As males carry only a single copy of the X chromosomes, selection is more effective for recessive mutations located on the X chromosome (Charlesworth, Coyne, and Barton 1987; Aquadro, Begun, and Kindahl 1994). Assuming that African populations (and urban populations in particular [see above]) are challenged by a continuous influx of non-African alleles, and these alleles are recessive and deleterious in Zimbabwean flies, selection will remove non-African alleles more efficiently on the X chromosome than on the autosomes. Thus, European alleles are maintained for longer time spans on the autosomes, leading to a higher proportion of European alleles on the autosomes. Irrespective of the selective force acting, hemizygosity of X chromosomes in males could therefore explain the observed difference between X chromosomes and autosomes.
Alternatively, if the number of European alleles deleterious in Zimbabwe is higher on the X chromosome, this could also explain the sheer absence of European alleles on the Zimbabwean X chromosomes. This hypothesis seems, however, unlikely given that X chromosomal gene density is not higher than the autosomal gene density (Hey and Kliman 2002). Finally, a higher impact of selection on the X chromosome could be due to stronger epistatic interactions on the X chromosome.
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Acknowledgements |
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Footnotes |
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