Male-Biased Mutation Rate and Divergence in Autosomal, Z-Linked and W-Linked Introns of Chicken and Turkey

Abstract

To investigate mutation-rate variation between autosomes and sex chromosomes in the avian genome, we have analyzed divergence between chicken (Gallus gallus) and turkey (Meleagris galopavo) sequences from 33 autosomal, 28 Z-linked, and 14 W-linked introns with a total ungapped alignment length of approximately 43,000 bp. There are pronounced differences in the mean divergence among autosomes and sex chromosomes (autosomes [A] = 10.08%, Z chromosome = 10.99%, and W chromosome = 5.74%), and we use these data to estimate the male-to-female mutation-rate ratio (alpha(m)) from Z/A, Z/W, and A/W comparisons at 1.71, 2.37, and 2.52, respectively. Because the alpha(m) estimates of the three comparisons do not differ significantly, we find no statistical support for a specific reduction in the Z chromosome mutation rate (Z reduction estimated at 4.89%, P = 0.286). The idea of mutation-rate reduction in the sex chromosome hemizygous in one sex (i.e., X in mammals, Z in birds) has been suggested on the basis of theory on adaptive mutation-rate evolution. If it exists in birds, the effect would, thus, seem to be weak; a preliminary power analysis suggests that it is significantly less than 18%. Because divergence may vary within chromosomal classes as a result of variation in mutation and/or selection, we developed a novel double-bootstrapping method, bootstrapping both by introns and sites from concatenated alignments, to estimate confidence intervals for chromosomal class rates and for alpha(m). The narrowest interval for the alpha(m) estimate is 1.88 to 2.97 from the Z/W comparison. We also estimated alpha(m) using maximum likelihood on data from all three chromosome classes; this method yielded alpha(m) = 2.47 and approximate 95% confidence intervals of 2.27 to 2.68. Our data are broadly consistent with the idea that mutation-rate differences between chromosomal classes can be explained by the male mutation bias alone.

Z chromosome divergence, polymorphism and relative effective population size in a genus of lekking birds

“…Male biased mutation may also impact N eZ /N eA ratios as the numbers of cell divisions in the male germline are much higher than in the female germline (Haldane, 1935;Miyata et al, 1987;Axelsson et al, 2004). While there is mixed evidence of an evolved compensatory effect for hemizygous sex chromosomes generally, the study by Axelsson et al (2004) did not find this to be significant in galliform birds and estimated a male-to-female mutation rate ratio (α m ) of~2-fold based on three different methods. As π Z / π A is proportional to μ Z /μ A , allowing for higher male mutation rates will further lower N eZ /N eA ratios because Z chromosomes are more often found in males than females.…”

“…Estimating the allele frequency spectrum of the two species with larger sample sizes could help infer past bottlenecks (Allendorf et al, 2010). Male biased mutation may also impact N eZ /N eA ratios as the numbers of cell divisions in the male germline are much higher than in the female germline (Haldane, 1935;Miyata et al, 1987;Axelsson et al, 2004). While there is mixed evidence of an evolved compensatory effect for hemizygous sex chromosomes generally, the study by Axelsson et al (2004) did not find this to be significant in galliform birds and estimated a male-to-female mutation rate ratio (α m ) of~2-fold based on three different methods.…”

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

“…ensembl.org/Gallus_gallus), GenBank (www.embl.org), a previous study (Axelsson et al 2004), or sequencing (for details, see Supplemental information). To identify intronic sequence, we first BLASTed chicken cDNA sequences against the draft human genome at National Center for Biotechnology Information (NCBI; www.ncbi.nlm.nih.gov).…”

“…Many genomic features that differ between micro-and macrochromosomes have been implicated in causing mutation rate variation (Caron et al 2001;EyreWalker and Hurst 2001;IHGSC 2001;Lercher et al , 2003Lercher et al , 2004MGSC 2002;Axelsson et al 2004;Chuang and Li 2004;. Studies in mammals report a positive cor-relation between GC content and both substitution rate (EyreWalker 1993;Bielawski et al 2000;Williams and Hurst 2000;Smith et al 2002) and levels of genetic variation (Sachidanandam et al 2001).…”

Fluctuating fire regimes and their historical effects on genetic variation in an endangered shrubland specialist

“…To scale nuclear loci among themselves, we used the avian rate of 0.00195 substitutions/lineage/million years for sex‐linked genes and 0.00184 for autosomal genes (Axelsson et al. 2004) with relaxed clocks with a standard deviation of 0.45. To transform N e into absolute number of breeding individuals, we divided the population size estimate by generation time (Heled and Drummond 2008) assuming the age of reproduction of BCVI females to be 1 year (Grzybowski 1990).…”