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Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution.

ABSTRACT: The human X chromosome exhibits four "evolutionary strata," interpreted to represent distinct steps in the process whereby recombination became arrested between the proto X and proto Y. To test if this is a general feature of sex chromosome evolution, we studied the Z-W sex chromosomes of birds, which have female rather than male heterogamety and evolved from a different autosome pair than the mammalian X and Y. Here we analyze all five known gametologous Z-W gene pairs to investigate the "strata" hypothesis in birds. Comparisons of the rates of synonymous substitution and intronic divergence between Z and W gametologs reveal the presence of at least two evolutionary strata spread over the p and q arms of the chicken Z chromosome. A phylogenetic analysis of intronic sequence data from different avian lineages indicates that Z-W recombination ceased in the oldest stratum (on Zq; CHD1Z, HINTZ, and SPINZ) 102-170 million years ago (MYA), before the split of the Neoaves and Eoaves. However, recombination continued in the second stratum (on Zp; UBAP2Z and ATP5A1Z) until after the divergence of extant avian orders, with Z and W diverging 58-85 MYA. Our data suggest that progressive and stepwise cessation of recombination is a general feature behind sex chromosome evolution.

SUBMITTER: Handley LJ

PROVIDER: S-EPMC1470863 | biostudies-other | 2004 May

REPOSITORIES: biostudies-other

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Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution.

Handley Lori-Jayne Lawson LJ Ceplitis Helene H Ellegren Hans H

Genetics 20040501 1

The human X chromosome exhibits four "evolutionary strata," interpreted to represent distinct steps in the process whereby recombination became arrested between the proto X and proto Y. To test if this is a general feature of sex chromosome evolution, we studied the Z-W sex chromosomes of birds, which have female rather than male heterogamety and evolved from a different autosome pair than the mammalian X and Y. Here we analyze all five known gametologous Z-W gene pairs to investigate the "strat ...[more]

PMID: 15166161

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Project description:Snakes exhibit genetic sex determination, with female heterogametic sex chromosomes (ZZ males, ZW females). Extensive cytogenetic work has suggested that the level of sex chromosome heteromorphism varies among species, with Boidae having entirely homomorphic sex chromosomes, Viperidae having completely heteromorphic sex chromosomes, and Colubridae showing partial differentiation. Here, we take a genomic approach to compare sex chromosome differentiation in these three snake families. We identify homomorphic sex chromosomes in boas (Boidae), but completely heteromorphic sex chromosomes in both garter snakes (Colubridae) and pygmy rattlesnake (Viperidae). Detection of W-linked gametologs enables us to establish the presence of evolutionary strata on garter and pygmy rattlesnake sex chromosomes where recombination was abolished at different time points. Sequence analysis shows that all strata are shared between pygmy rattlesnake and garter snake, i.e., recombination was abolished between the sex chromosomes before the two lineages diverged. The sex-biased transmission of the Z and its hemizygosity in females can impact patterns of molecular evolution, and we show that rates of evolution for Z-linked genes are increased relative to their pseudoautosomal homologs, both at synonymous and amino acid sites (even after controlling for mutational biases). This demonstrates that mutation rates are male-biased in snakes (male-driven evolution), but also supports faster-Z evolution due to differential selective effects on the Z. Finally, we perform a transcriptome analysis in boa and pygmy rattlesnake to establish baseline levels of sex-biased expression in homomorphic sex chromosomes, and show that heteromorphic ZW chromosomes in rattlesnakes lack chromosome-wide dosage compensation. Our study provides the first full scale overview of the evolution of snake sex chromosomes at the genomic level, thus greatly expanding our knowledge of reptilian and vertebrate sex chromosomes evolution.

Project description:BackgroundX chromosome inactivation is the transcriptional silencing of one X chromosome in the somatic cells of female mammals. In eutherian mammals (e.g. humans) one of the two X chromosomes is randomly chosen for silencing, with about 15% (usually in younger evolutionary strata of the X chromosome) of genes escaping this silencing. In contrast, in the distantly related marsupial mammals the paternally derived X is silenced, although not as completely as the eutherian X. A chromosome wide examination of X inactivation, using RNA-seq, was recently undertaken in grey short-tailed opossum (Monodelphis domestica) brain and extraembryonic tissues. However, no such study has been conduced in Australian marsupials, which diverged from their American cousins ~80 million years ago, leaving a large gap in our understanding of marsupial X inactivation.ResultsWe used RNA-seq data from blood or liver of a family (mother, father and daughter) of tammar wallabies (Macropus eugenii), which in conjunction with available genome sequence from the mother and father, permitted genotyping of 42 expressed heterozygous SNPs on the daughter's X. These 42 SNPs represented 34 X loci, of which 68% (23 of the 34) were confirmed as inactivated on the paternally derived X in the daughter's liver; the remaining 11 X loci escaped inactivation. Seven of the wallaby loci sampled were part of the old X evolutionary stratum, of which three escaped inactivation. Three loci were classified as part of the newer X stratum, of which two escaped inactivation. A meta-analysis of previously published opossum X inactivation data revealed that 5 of 52 genes in the old X stratum escaped inactivation.ConclusionsWe demonstrate that chromosome wide inactivation of the paternal X is common to an Australian marsupial representative, but that there is more escape from inactivation than reported for opossum (32% v 14%). We also provide evidence that, unlike the human X chromosome, the location of loci within the oldest evolutionary stratum on the marsupial X does not correlate with their probability of escape from inactivation.

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Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution.

Publications

Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution.

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