Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes

Axelsson, Erik; Webster, Matthew T.; Smith, Nick G.C.; Burt, David W.; Ellegren, Hans

doi:10.1101/gr.3021305

Cited by 145 publications

(147 citation statements)

References 58 publications

(47 reference statements)

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“…Importantly, the d N /d S ratio was still significantly higher (P = 0.04) in the Z-linked genes (0.110) than in genes that mapped to chicken chromosomes 1-10 (0.0948). The reduction in d S for chromosomes 1-10 compared to all autosomes is consistent with previous observations of a lower mutation rate on macro-than on microchromosomes (International Chicken Genome Sequencing Consortium 2004; Axelsson et al 2005). This seems largely because of the higher GC content of microchromosomes and the positive correlation between GC and substitution rate in birds (Webster et al 2006).…”

Section: Divergence Datasupporting

confidence: 80%

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

Mank¹,

Axelsson²,

Ellegren³

2007

Genome Res.

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150

132

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Theoretical work predicts natural selection to be more efficient in the fixation of beneficial mutations in X-linked genes than in autosomal genes. This "fast-X effect" should be evident by an increased ratio of nonsynonymous to synonymous substitutions (d N /d S ) for sex-linked genes; however, recent studies have produced mixed support for this expectation. To make an independent test of the idea of fast-X evolution, we focused on birds, which have female heterogamety (males ZZ, females ZW), where analogous arguments would predict a fast-Z effect. We aligned 2.8 Mb of orthologous protein-coding sequence of zebra finch and chicken from 172 Z-linked and 4848 autosomal genes. Zebra finch data were in the form of EST sequences from brain cDNA libraries, while chicken genes were from the draft genome sequence. The d N /d S ratio was significantly higher for Z-linked (0.110) than for all autosomal genes (0.085; P = 0.002), as well as for genes linked to similarly sized autosomes 1-10 (0.0948; P = 0.04). This pattern of fast-Z was evident even after we accounted for the nonrandom distribution of male-biased genes. We also examined the nature of standing variation in the chicken protein-coding regions. The ratio of nonsynonymous to synonymous polymorphism (p N /p S ) did not differ significantly between genes on the Z chromosome (0.104) and on the autosomes (0.0908). In conjunction, these results suggest that evolution proceeds more quickly on the Z chromosome, where hemizygous exposure of beneficial nondominant mutations increases the rate of fixation.[Supplemental material is available online at www.genome.org and http://www.egs.uu.se/evbiol/Research/Data/fast-Z/.] Sex chromosomes can exhibit several unusual properties, including inheritance pattern, reduced recombination, and hemizygosity, which influence the mechanisms of natural selection (Rice 1984; Vicoso and Charlesworth 2006). These differences often make evolutionary comparisons between sex chromosomes and autosomes particularly revealing, as they help answer fundamental questions regarding the signature and pattern of mutation and natural selection, as well as how these forces vary across the genome. For instance, consider new autosomal mutations, which are initially low in frequency and primarily present in heterozygotes. If these mutations are either wholly or partially recessive, they will be obscured by the ancestral allele, and will only rarely be exposed directly to selective forces. In contrast, novel recessive and otherwise nondominant mutations on sex chromosomes are directly exposed to selection in the hemizygous sex. Selection would therefore be expected to act faster on sex chromosomes to fix some types of beneficial mutations (Charlesworth et al. 1987), a situation referred to as fast-X evolution.The fast-X (or fast-Z in the case of female heterogamety) effect could potentially explain several evolutionary phenomena. For instance, it has been invoked to explain Haldane's Rule (Haldane 1922), which states that the heterogametic sex suffers highe...

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Section: Divergence Datasupporting

confidence: 80%

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

Mank¹,

Axelsson²,

Ellegren³

2007

Genome Res.

Self Cite

150

132

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“…Specifically, we found that K S distribution differences between genes on chicken micro-and macrochromosomes also remain significant when only considering genes exhibiting similar G+C contents, or G+C percentage at fourfold degenerate sites 126 (Table 9). Higher neutral divergence rates are also seen on microchromosomes when genes are compared between chicken and turkey genomes 127 . Second, subtelomeric sequences, which are often duplicated and polymorphic 86,128 , also show elevated neutral substitution rates.…”

Section: Synonymous Substitution Ratesmentioning

confidence: 93%

Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution

2004

Nature

2,241

1,052

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“…Both chicken and turkey belong to the order Galliformes and show a neutral autosomal sequence divergence of $10% (Axelsson et al 2005). We found 11,011 interspecific indels in the alignments after filtering for repetitive arrays using the same criteria as in the polymorphism data set.…”

Section: à13mentioning

confidence: 89%

The Genomic Landscape of Short Insertion and Deletion Polymorphisms in the Chicken (Gallus gallus) Genome: A High Frequency of Deletions in Tandem Duplicates

Brandström

Ellegren

2007

Genetics

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It is increasingly recognized that insertions and deletions (indels) are an important source of genetic as well as phenotypic divergence and diversity. We analyzed length polymorphisms identified through partial (0.253) shotgun sequencing of three breeds of domestic chicken made by the International Chicken Polymorphism Map Consortium. A data set of 140,484 short indel polymorphisms in unique DNA was identified after filtering for microsatellite structures. There was a significant excess of tandem duplicates at indel sites, with deletions of a duplicate motif outnumbering the generation of duplicates through insertion. Indel density was lower in microchromosomes than in macrochromosomes, in the Z chromosome than in autosomes, and in 100 bp of upstream sequence, 59-UTR, and first introns than in intergenic DNA and in other introns. Indel density was highly correlated with single nucleotide polymorphism (SNP) density. The mean density of indels in pairwise sequence comparisons was 1.9 3 10 À4 indel events/bp, $5% the density of SNPs segregating in the chicken genome. The great majority of indels involved a limited number of nucleotides (median 1 bp), with A-rich motifs being overrepresented at indel sites. The overrepresentation of deletions at tandem duplicates indicates that replication slippage in duplicate sequences is a common mechanism behind indel mutation. The correlation between indel and SNP density indicates common effects of mutation and/or selection on the occurrence of indels and point mutations.

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Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes

Cited by 145 publications

References 58 publications

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution

The Genomic Landscape of Short Insertion and Deletion Polymorphisms in the Chicken (Gallus gallus) Genome: A High Frequency of Deletions in Tandem Duplicates

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