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Global Patterns of Human Mitochondrial DNA and Y-Chromosome Structure Are Not Influenced by Higher Migration Rates of Females Versus Males

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Global Patterns of Human Mitochondrial DNA and Y-Chromosome Structure Are Not Influenced by Higher Migration Rates of Females Versus Males LETTERS Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males Jason A Wilder1,2, Sarah B Kingan1, Zahra Mobasher1, Maya Metni Pilkington3 & Michael F Hammer1,2 Global-scale patterns of human population structure may be have adopted a strategy6–9 to estimate levels of between-group varia- influenced by the rate of migration among populations that is tion using single-nucleotide polymorphisms (SNPs) discovered in nearly eight times higher for females than for males. This small panels of globally diverse males and then genotyped in much http://www.nature.com/naturegenetics difference is attributed mainly to the widespread practice of larger population samples (e.g., the global data set10 analyzed in ref. 1). patrilocality, in which women move into their mates’ This nonrandom sampling of SNPs can result in an ascertainment 1 residences after marriage . Here we directly test this bias that has an unknown effect on estimates of FST values. hypothesis by comparing global patterns of DNA sequence Several researchers have suggested that an extensive study of variation on the Y chromosome and mitochondrial DNA mtDNA and Y-chromosome diversity in the same samples, using (mtDNA) in the same panel of 389 individuals from ten the same method to assay variation, is necessary before one can make populations (four from Africa and two each from Europe, firm conclusions regarding the relative degree of mtDNA and Asia and Oceania). We introduce a new strategy to assay Y-chromosome differentiation4,11. Y-chromosome variation that identifies a high density of single- Here, we directly compare 6.7 kb of Y-chromosome sequence and nucleotide polymorphisms, allows complete sequencing of all 770 bp of the gene mitochondrial cytochrome c oxidase 3 (MTCO3)in individuals rather than relying on predetermined markers and a sample of 389 individuals representing ten globally distributed provides direct sequence comparisons with mtDNA. We found human populations. We assayed Y-chromosome variation using the overall proportion of between-group variation (UST)tobe DNA sequences that encompass recently inserted Alu retrotransposons © 2004 Nature Publishing Group 0.334 for the Y chromosome and 0.382 for mtDNA. Genetic differentiation between populations was similar for the Y chromosome and mtDNA at all geographic scales that we Table 1 Characteristics of individual Alu elements sequenced on the tested. Although patrilocality may be important at the local Ychromosome scale2,3, patterns of genetic structure on the continental and Alu Alu Gene region Length, including Segregating global scales are not shaped by the higher rate of migration name family (intron number) flanking DNA (bp) sites among females than among males. 16e4 Ya5SMCY(14)4226 Differences in migration rates between males and females can be 486 Ya5 DFFRY (31) 290 4 inferred from analyses of within- and between-group variation (e.g., DBYc2 Yc2 DBY (2) 340 2 FST, a measure of genetic differentiation among populations) for the DBYd1 Yd2 DBY (2) 588 2 maternally inherited mtDNA and paternally inherited Y chromosome. AMELY Y AMELY (2) 734 6 Using this approach, one study pieced together data sets from DFFRY30 Y DFFRY (11) 663 5 published mtDNA, Y-chromosome and autosomal studies and DFFRY40 Y DFFRY (13) 546 6 found that the Y chromosome had larger between-group differences DFFRY50 Y DFFRY (17) 413 1 than did other portions of the genome1. But these data sets varied SMCY2 Y SMCY (5) 406 1 considerably with regard to sample sizes, populations represented and UTY62 Y UTY (10) 525 3 method used to assay genetic variation4, making any comparison of UTY87 Y UTY (19) 440 1 the extent of genetic differentiation between populations difficult. This DFFRY04 Y DFFRY (1) 520 2 UTY83 Y UTY (19) 796 4 problem is exacerbated for Y chromosomes because they lack sequence Total 6,683 43 diversity5. To accommodate this difficulty, Y-chromosome researchers 1Division of Biotechnology, 2Department of Ecology and Evolutionary Biology and 3Department of Anthropology, University of Arizona, Tucson, Arizona 85721, USA. Correspondence should be addressed to M.F.H. ([email protected]). Published online 19 September 2004; doi:10.1038/ng1428 1122 VOLUME 36 [ NUMBER 10 [ OCTOBER 2004 NATURE GENETICS LETTERS Table 2 AMOVA results for the Y chromosome and mtDNA at global values for mtDNA than for the Y chromosome (Table 2). The and continental scales between-groups component of genetic variation was higher for mtDNA than for the Y chromosome in every region except Asia, Variation Variation between where the Y-chromosome FST value slightly exceeded that of mtDNA Geographic region within groups (%) groups (%) (by 0.002). An AMOVA that incorporated a hierarchical grouping of Global (10 populations) populations within continents yielded similar results (Table 3). Values Y chromosome 66.5 33.4 of FSC (between-group, within-continent variation) and FCT mtDNA 62.0 38.2 (between-continent variation) were similar for mtDNA and the Africa (4 populations) Y chromosome, though slightly higher for mtDNA. Y chromosome 79.2 20.8 In addition to the overall similarity of between-group components mtDNA 68.0 32.0 of variation for the Y chromosome and mtDNA, there was a strong Non-Africa (6 populations) and statistically significant correlation of FST values between pairs Y chromosome 76.2 23.8 of populations for these loci (Fig. 1; Mantel correlation coefficient mtDNA 73.0 27.0 ¼ 0.688; P o 0.001). This result has several important implications. Asia (2 populations) First, it indicates that putative gene flow among populations is Ychromosome 97.4 2.6 relatively symmetrical for females and males. The fact that FST mtDNA 97.7 2.3 values for these loci covary so strongly suggests that population- Oceania (2 populations) specific processes, such as variation in rates of migration for females Y chromosome 79.5 20.5 versus males, do not influence our divergence data. Second, it mtDNA 60.9 39.1 indicates that there is no obvious trend towards different rates of Europe (2 populations) divergence for mtDNA versus the Y chromosome. Although the Ychromosome 101.1 À1.1 nonindependence of the data points in Figure 1 precludes conven- mtDNA 100.5 À0.5 http://www.nature.com/naturegenetics tional statistical analyses, we noted that the slope of the regression line suggests a faster increase in divergence between populations for mtDNA than for the Y chromosome, contrary to the pattern (e.g., the Y family of Alu elements and its subfamilies12; Table 1), that would be expected if females had a higher rate of migration. because these elements may have a higher mutation rate than other Finally, the strong correlation between FST values for these two noncoding DNA as a result of their high density of CpG dinucleo- compartments of the genome indicates that demographic, rather tides13. Focusing on these regions, we uncovered a much higher than locus-specific, evolutionary forces are the primary determinants density of SNPs than reported in previous surveys. SNP density was of genetic distance between the populations we surveyed. Positive 3.15 times higher in our data set than in a study of a pseudogene and directional selection, for instance, operating in a subset of popula- other noncoding regions on the Y chromosome5 (comparing data tions on either the Y chromosome or mtDNA would tend to uncouple from 73 individuals that overlap between the two studies). Given the FST values between loci. We see no evidence for such a process in value of Watterson’s y (an estimator of the quantity 2Nem, where Ne is our data. the effective population size and m is the mutation rate) in our present Our survey of the Y chromosome and mtDNA found markedly © 2004 Nature Publishing Group Alu data set, we estimated the probability of observing a SNP density different between-group components of variation than have been equal to or lower than that observed in the non-Alu data set to be P ¼ reported in previous global studies. Some Y-chromosome studies 0.007 using coalescent simulations. Thus, there is a significant increase rely on predetermined SNPs and find that between-population com- in DNA sequence variation in regions encompassing Alu elements over ponents of genetic variation are much higher than we estimated1,11. the background level of noncoding diversity on the Y chromosome. Our data suggest that ascertainment biases associated with the use of Using this rich source of polymorphism, we can directly compare particular SNPs may result in overestimates of genetic distance sequence variation between the Y chromosome and mtDNA in a between populations. In contrast, previous studies of mtDNA often manner that is free of ascertainment bias for both loci. We observed 43 focus on hypervariable portions of the control region (where high Y-chromosome SNPs and 68 mtDNA SNPs (Supplementary Tables 1 mutation rates may cause a downward bias in estimates of between- and 2 online). group variation15) rather than coding DNA11.Weobtainedmuch We found no evidence that the Y chromosome has a higher level of higher estimates of between-group variation when we compared differentiation between populations than does mtDNA. Using an mtDNA coding sequences with hypervariable regions in the same analysis of molecular variance (AMOVA), we calculated the overall panel of individuals (Supplementary Note online). value of FST (which approximates the quantity 1/(1 + Nem) assuming Our interpretation of the between-group components of genetic an equilibrium island model of population structure14,wherem is the variation for the Y chromosome and mtDNA in terms of rates of migration rate between populations) to be 0.334 for the Y chromo- migration relies on the assumption that the effective population sizes some and 0.382 for mtDNA.
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