Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden
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Abstract |
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Introduction |
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Comparative analyses of the degree of nucleotide diversity on sex chromosomes may offer a useful context for studying the effects of local variation in the mutation rate on levels of genetic variability. The two distinct types of sex chromosomes found in most vertebrates (e.g., X and Y in mammals, and Z and W in birds) may inherently be associated with different mutation rates given that they spend different amounts of time in male and female germ lines (Miyata et al. 1987
). Producing a massive amount of sperm, male germ cells undergo many more mitotic cell divisions prior to fertilization than do female germ cells, and, assuming DNA replication to be an important source of mutation, this would lead to a male bias in the mutation rate. Indeed, there are several lines of evidence from different taxonomic groups that males mutate more often than females (Miyata et al. 1987
; Shimmin, Chang, and Li 1993
; Ellegren and Fridolfsson 1997
; Hurst and Ellegren 1998
; Kahn and Quinn 1999
; Ellegren 2000a
), and a male-biased mutation rate should translate into biased mutation pressures on the two sex chromosomes. In mammals, the Y chromosome is only transmitted from fathers to sons, and thus Y-linked mutations arise only in the male germ line. The X chromosome, on the other hand, spends two thirds of its time in the female germ line, and, in a predictable manner, the frequency of X-linked mutations should therefore reflect a combination of male- and female-specific mutation rates. In line with this expectation, presumably neutral sequences on the Y chromosomes of primates and other mammals have been shown to evolve faster than paralogous sequences on the X chromosome (Miyata et al. 1987
; Shimmin, Chang, and Li 1993
; Chang et al. 1994
; Huang et al. 1997
; Agulnik et al. 1997
; Pecon Slattery and O'Brien 1998
). Similarly, in birds, in which males are homogametic ZZ and females are heterogametic ZW, presumably neutral sequences on the Z chromosome have been shown to evolve faster than paralogous sequences on the female-specific W chromosome (Ellegren and Fridolfsson 1997
; Kahn and Quinn 1999
; Carmichael et al. 2000
; Fridolfsson and Ellegren 2000
).
If the mutation rate is male-biased and, as a consequence, the mutation rate is higher on the sex chromosome which spends most of its time in male germ line (i.e., Z in birds), we should expect higher levels of genetic variability on this sex chromosome than on the other, other things being equal. In theory, however, other things might not be identical. For instance, the heteromorphic, sex-limited sex chromosome has a smaller effective population size (typically one third that of the other sex chromosome) and does not undergo recombination outside of the pseudoautosomal region. These are factors generally associated with lowered levels of polymorphism (Maynard-Smith and Haigh 1974
), and they thus need to be taken into account when interpreting levels of genetic variability on sex chromosomes.
In this study, we analyzed the degree of nucleotide diversity in two sex-linked avian genes, CHD1Z (chromo-helicase-DNA-binding protein 1 on the Z chromosome) and CHD1W (its homolog on the W chromosome). Representing two independently evolving paralogs (Fridolfsson and Ellegren 2000
; Garcia-Moreno and Mindell 2000
) exposed to different genomic environments, the avian CHD1 genes offer the possibility to unveil the effect of varying mutation rates on degree of genetic variability. We also discuss the data in the context of possible effects of selection.
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Materials and Methods |
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PCR Amplification
The complete exon-intron structure of avian CHD1 genes has not been elucidated; hence, we arbitrarily designated the introns studied herein intron A and intron B. For CHD1W, intron A was amplified using primers 2464F (ATACTTGAAGTATGGTCAGTT) and 2781R (Fridolfsson and Ellegren 1999
), and intron B was amplified using primers 2987F and 3112R (Ellegren and Fridolfsson 1997
); these primer pairs consistently revealed W-specific amplification. For CHD1Z, the corresponding introns were amplified with primers 2550F (Ellegren and Fridolfsson 1997
) and 2781R and with 3007F (Fridolfsson and Ellegren 1999
) and 3112R, respectively. Amplification products obtained with these primers contained short parts of exonic sequence in their ends. Unless otherwise stated, these were excluded from analyses. The 20-µl PCR reactions contained 0.2 µM of each primer, 0.2 µM dNTP, 0.04 U AmpliTaq (Perkin Elmer; AmpliTaq Gold for primer pair 2464F-2781R), 1 x AmpliTaq buffer, and 2050 ng DNA. The MgCl2 concentrations used in the reactions were 3 mM for CHD1W intron A, 2.5 mM for CHD1Z intron A, and 2 mM for the others. The following PCR profiles were used in a Perkin-Elmer 9600 thermo cycler: 2987F-3112R and 3007F-3112R95°C for 2 min, 3 x (94°C for 30 s, 60°C for 30 s, and 72°C for 30 s), 29 x (94°C for 30 s, 55°C for 30 s, and 72°C for 30 s); 2464F-2781R95°C for 5 min, 62°C for 30 s, and 72°C for 20 s, 10 x (94°C for 40 s, touchdown 6052°C for 30 s [decreasing 1°C/cycle], and 72°C for 30 s), 35 x (94°C for 30 s, 50°C for 30 s, and 72°C for 40 s); 2550F-2781R95°C for 2 min, 5 x (94°C for 30 s, touchdown 6052°C for 30 s [decreasing 2°C/cycle], and 72°C for 30 s), 27 x (94°C for 30 s, 55°C for 30 s, and 72°C for 50 s). All programs were ended with an extended elongation step of 72°C for 5 min.
Single-Strand Conformation Polymorphism Analysis
PCR products were analyzed for sequence variation using single-strand conformation polymorphism (SSCP). Prior to electrophoresis, 2 µl of PCR product was mixed with 6 µl formamide containing loading buffer, denatured at 96°C for 3 min, and kept on ice. Twelve percent polyacrylamide gels were run at 1 W for 2124 h at 20°C and then silver-stained. The silver staining procedure involved fixation in 10% acetic acid for 20 min, two washes in deionized water, staining in 1 g/liter AgNO3 for 40 min, a short wash in deionized water, and development in Na2CO3 until bands were clearly visible.
Cloning and Sequencing
PCR products of heterozygous males and occasionally also of other templates were cloned. This was done either by blunt-ending and dephosphorylation of PCR products, followed by ligation into SmaI cut pUC18 plasmids, or by using the pGEM T-vector kit from Promega. The identities of inserts were tested by PCR with original primers, and appropriate plasmid DNAs were subsequently purified using a Miniprep kit (Saveen). Plasmids and PCR products (the latter of which had been purified by Qiaquick columns; Qiagen) were cycle-sequenced with BigDye terminator chemistry and analyzed on an ABI 377 automated sequencer (Perkin-Elmer). All sequences observed in this study have been submitted to GenBank under accession numbers AF294630AF294645 and AF364551AF364558.
Data Analysis
DNA sequences were edited and aligned in the programs Sequencher 3.0 (Gene Codes Corp.) and Sequence Navigator 1.0 (Applied Biosystems). Estimates of nucleotide diversity ( and
) were obtained and HKA tests (Hudson, Kreitman, and Aguadé 1987
) for departure from neutrality were performed using the program DnaSP 3.0 (Rozas and Rozas 1999
). The HKA test is a test that relates intraspecific polymorphism at two loci (in this case, CHD1Z and CHD1W) to interspecific divergence at the same two loci. Resampling of sequences and sites was performed using a program written in C++. The proportion of subsamples having more than zero segregating sites was used as the probability that the level of polymorphism was higher on the Z chromosome than on the W chromosome. Probabilities from individual species were combined according to Sokal and Rohlf (2000
, p. 795).
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Results |
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Levels of genetic variability at the Z and W chromosomes may not be directly comparable, since nucleotide diversity in neutral DNA sequences is also governed by the effective population size (Crow and Kimura 1970
). With an infinite-sites model,
equals nNeu, where n is the number of haploid sets of chromosomes per breeding pair, Ne is the effective population size, and u is the mutation rate. For the avian Z and W sex chromosomes, n is 3 and 1, respectively. We should thus expect genetic variability on Z to be three times as high as that on W merely due to this fact. Correcting for effective population size (i.e., dividing variability estimates by three),
corr and
corr for CHD1Z introns became 0.00066 and 0.00070, respectively. It is difficult to quantify the relative excess of polymorphism on the Z chromosome compared with the W chromosome given that the latter was monomorphic in our sample. If there had been a single rare allele (e.g., a frequency of 5%) in one of the surveyed W chromosome introns, we would have arrived at
and
values of approximately 0.00004 and 0.00010, respectively, for the W chromosome. We thus conclude that our data suggest the degree of genetic variability on the avian Z chromosome to be at least about 10 times as high as that on the W chromosome, even when effective population size has been corrected for. However, it should be noted that we cannot formally support this quantitative statement with statistical evidence, as there was no variation on the W chromosome.
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Discussion |
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It is thus difficult to evaluate the possible role of selection based on our sequence data. Are there other lines of evidence which might argue for or against an effect from selection at linked loci on the W chromosome? Relevant to this question is the fact that it is unclear if the avian W chromosome contains a sex-determining locus (Raymond et al. 1999
; Smith et al. 1999
; Ellegren 2000b, 2001
). Overall, the nonrecombining part of the avian W chromosome contains very few coding sequences (Ellegren 2000b
). Only three expressed genes have so far been identified across avian lineages: CHD1W (Ellegren 1996
; Griffiths, Daan, and Dijkstra 1996
), the
subunit of ATP synthase (ATP5A1W; Dvorák et al. 1992
; Fridolfsson et al. 1998
), and a modified variant of the protein kinase C inhibitor PKCIW (Hori et al. 2000
; O'Neill et al. 2000
). Although it is difficult to make a quantitative assessment, this suggests that the deleterious mutation rate of the avian W chromosome may not be high enough for background selection to reduce nucleotide diversity (cf. Charlesworth, Morgan, and Charlesworth 1993
; Nachman 1998
; Zuruvcova and Eanes 1999). Moreover, two of the three W-linked genes (CHD1W and ATP5A1W) have paralogs on the Z chromosome which are very similar on the amino acid level (97%98% identity for CHD1), as well as on the nucleotide level (the frequency of nonsynonymous substitutions is 0.0150.02 for CHD1; Fridolfsson and Ellegren 2000
; Carmichael et al. 2000
). This may suggest that CHD1Z and CHD1W, as well as ATP5A1Z and ATP5A1W, share functional properties to the extent that these gene pairs could in fact be seen as allelic variants of the same proteins. In line with this, an analysis of the molecular evolution of CHD1W provided no evidence for positive selection (Fridolfsson and Ellegren 2000
), which would have been suggestive of a female-specific role. If these observations represent a general pattern for W-linked genes in birds, selective sweeps may not be a common feature shaping the degree of genetic variability on the avian W chromosome.
Effects of Reproduction and Migration
In theory, reproductive skewness (sexual selection) and female migration could cause rapid spread of W chromosomes, thereby acting to reduce the levels of genetic variability on W relative to Z. However, polyandry, leading a few females to mother a disproportionally large number of offspring, is rare among birds (Waite and Parker 1997; Ligon 1999
). Indeed, male passerine birds generally tend to be more philopatric than females (Clarke, Saether, and Roskaft 1997
), but the overall picture for many species, including at least the barn swallow (Møller 1994
) and the collared flycatcher (Pärt 1995
) analyzed in this study, is that of weak dispersal among both sexes. Therefore, reproduction and migration can likely be ruled out as being important in this context.
Genetic Variability of X and Y Sex Chromosomes
While this is the first report of contrasting levels of genetic variability on the two sex chromosomes of organisms with female heterogamety (ZW), such data are available for some organisms with male heterogamety (XY). Among the latter, we might expect higher levels of genetic variability on the Y than on the X chromosome (corrected for the difference in effective population size) if the mutation rate is male-biased. However, several reports have pointed in the opposite direction. For instance, genetic variability of the human Y chromosome has been claimed to be low (Jakubiczka et al. 1989
; Ellis et al. 1990
; Malaspina et al. 1990
; Dorit, Akashi, and Gilbert 1995
; Jobling and Tyler-Smith 1995
; Whitfield, Sulston, and Goodfellow 1995
; Hammer et al. 1997
), a situation commonly attributed to the effect of selective sweeps. For example, a recent comparison of nucleotide diversity in a 16.5-kb region on the Y chromosome and in a 5-Mb region on the human X chromosome, with the latter using the solid-phase chemical mismatch-cleavage method, revealed a twofold deficit of variation on Y relative to X (Anagnostopoulos et al. 1999
; effective population size taken into account). However, it has been argued that the interpretation of selective sweeps lacks firm support, since most tests of neutrality of human Y-linked sequences fail to reject neutral models (Hammer 1995
). Indeed, some recent comparisons of several Y-linked, X-linked, and autosomal sequences indicate that there is at most only a modest reduction in human Y chromosome variability (Nachman 1998
; Jaruzelska, Zietkiewicz, and Labuda 1999
). Similar to our study, however, the low intraspecific variability typically seen in studies of the human Y chromosome will inevitably give low statistical power in HKA and Tajima tests (Nachman 1998
; Jaruzelska, Zietkiewicz, and Labuda 1999
). Perhaps there are intrinsic differences in the evolutionary rates of different Y chromosome sequences that can explain the varying results of different studies. For instance, it appears that both ZFY and ZFX evolve slowly and are unusually low in polymorphism (Hammer 1995
; Huang et al. 1998
; Jaruzelska, Zietkiewicz, and Labuda 1999
). However, an important conclusion from these studies is that the human Y chromosome is at least not associated with an unusually high degree of polymorphism, as would be predicted from a male-biased mutation rate.
Low levels of Y-chromosome variation have also been documented in other taxa. In the dioecious plant Silene latifolia, DNA polymorphism in a 2-kb genomic region of the Y-linked SLY-1 gene (including both exons and introns) was found to be 20-fold lower than in paralogous sequences of the X-linked SLX-1 gene (Filatov et al. 2000
). In Drosophila melanogaster and Drosophila simulans, nucleotide diversity in the Y-linked Dhc-Yh3 gene was about an order of magnitude less than that predicted from data on autosomal and X-linked sequences (Zurovcova and Eanes 1999
). The fact that the Drosophila Y chromosome has a low gene number led Zurovcova and Eanes (1999)
to favor adaptive sweeps as explaining the deficit of Y-chromosome variation. It should be noted that the mutation rate in Drosophila is probably not sex-biased (Bauer and Aquadro 1997
). In the Silene study, on the other hand, the pattern of nucleotide diversity in Y chromosome sequences (no singletons among polymorphic sites) was not consistent with selective sweeps (Filatov et al. 2000
).
Methodological Aspects
One potentially confounding factor affecting the degree of nucleotide diversity seen in this study is the efficiency of the SSCP technique in uncovering polymorphisms. Previous studies have suggested that SSCP analysis detects well above 80% of polymorphisms and in some cases as much as 98%, depending on fragment length (Hayashi 1991
; Hayashi and Yandell 1991
; Jaruzelska, Zietkiewicz, and Labuda 1999
). It seems reasonable to assume that SSCP efficiency should depend on sequence characteristics of the fragment being assayed. Importantly, since we analyzed Z- and W-chromosome fragments with significant sequence homology, it is difficult to see that the relative efficiency of SSCP detection could have been dramatically different for CHD1Z and CHD1Z introns. In fact, sequencing of 10 males and 10 females of both pied flycatcher and collared flycatcher did not uncover any additional polymorphisms compared with that detected with SSCP. Moreover, in addition to arguing against possible methodological artifacts, the use of homologous introns should also warrant that sequence-specific effects are avoided (e.g., due to distinctly different GC contents).
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Conclusions |
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Acknowledgements |
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Footnotes |
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1 Keywords: germ line
male bias
mutation
selective sweep
background selection
sex chromosomes
2 Address for correspondence and reprints: Hans Ellegren, Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. hans.ellegren{at}ebc.uu.se
.
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