Cargando…

Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation

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 complet...

Descripción completa

Detalles Bibliográficos
Autores principales: Vicoso, Beatriz, Emerson, J. J., Zektser, Yulia, Mahajan, Shivani, Bachtrog, Doris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3754893/
https://www.ncbi.nlm.nih.gov/pubmed/24015111
http://dx.doi.org/10.1371/journal.pbio.1001643
_version_ 1782281926944489472
author Vicoso, Beatriz
Emerson, J. J.
Zektser, Yulia
Mahajan, Shivani
Bachtrog, Doris
author_facet Vicoso, Beatriz
Emerson, J. J.
Zektser, Yulia
Mahajan, Shivani
Bachtrog, Doris
author_sort Vicoso, Beatriz
collection PubMed
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.
format Online
Article
Text
id pubmed-3754893
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-37548932013-09-06 Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation Vicoso, Beatriz Emerson, J. J. Zektser, Yulia Mahajan, Shivani Bachtrog, Doris PLoS Biol Research Article 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. Public Library of Science 2013-08-27 /pmc/articles/PMC3754893/ /pubmed/24015111 http://dx.doi.org/10.1371/journal.pbio.1001643 Text en © 2013 Vicoso et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Vicoso, Beatriz
Emerson, J. J.
Zektser, Yulia
Mahajan, Shivani
Bachtrog, Doris
Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title_full Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title_fullStr Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title_full_unstemmed Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title_short Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation
title_sort comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3754893/
https://www.ncbi.nlm.nih.gov/pubmed/24015111
http://dx.doi.org/10.1371/journal.pbio.1001643
work_keys_str_mv AT vicosobeatriz comparativesexchromosomegenomicsinsnakesdifferentiationevolutionarystrataandlackofglobaldosagecompensation
AT emersonjj comparativesexchromosomegenomicsinsnakesdifferentiationevolutionarystrataandlackofglobaldosagecompensation
AT zektseryulia comparativesexchromosomegenomicsinsnakesdifferentiationevolutionarystrataandlackofglobaldosagecompensation
AT mahajanshivani comparativesexchromosomegenomicsinsnakesdifferentiationevolutionarystrataandlackofglobaldosagecompensation
AT bachtrogdoris comparativesexchromosomegenomicsinsnakesdifferentiationevolutionarystrataandlackofglobaldosagecompensation