Independent Stratum Formation on the Avian Sex Chromosomes Reveals Inter‐chromosomal Gene Conversion and Predominance of Purifying Selection on the W Chromosome

Wright, Alison E.; Harrison, Peter W.; Montgomery, Stephen H.; Pointer, Marie A.; Mank, Judith E.

doi:10.1111/evo.12493

Cited by 55 publications

(67 citation statements)

References 99 publications

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“…3a) 7,18,21 . We stratified these candidate W-linked genes into two groups, based on the amount of information used to identify W-linked genes for each species.…”

Section: Resultsmentioning

confidence: 99%

Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators

et al. 2017

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After birds diverged from mammals, different ancestral autosomes evolved into sex chromosomes in each lineage. In birds, females are ZW and males ZZ, but in mammals females are XX and males XY. We sequenced the chicken W chromosome, compared its gene content with our reconstruction of the ancestral autosomes, and followed the evolutionary trajectory of ancestral W-linked genes across birds. Avian W chromosomes evolved in parallel with mammalian Y chromosomes, preserving ancestral genes through selection to maintain the dosage of broadly-expressed regulators of key cellular processes. We propose that, like the human Y chromosome, the chicken W chromosome is essential for embryonic viability of the heterogametic sex. Unlike other sequenced sex chromosomes, the chicken W did not acquire and amplify genes specifically expressed in reproductive tissues. We speculate that the pressures that drive the acquisition of reproduction related genes on sex chromosomes may be specific to the male germ line.

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“…3a) 7,18,21 . We stratified these candidate W-linked genes into two groups, based on the amount of information used to identify W-linked genes for each species.…”

Section: Resultsmentioning

confidence: 99%

Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators

et al. 2017

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“…Evolutionary strata are also found in bird sex chromosomes (Wright et al. ; Zhou et al. ), and two strata have been detected in both plant species whose X–Y sequence divergence has so far been studied, S. latifolia (Bergero et al.…”

Section: Sex Chromosomes As Supergenesmentioning

confidence: 99%

The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations

Charlesworth

2015

Evolutionary Applications

125

186

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I review theoretical models for the evolution of supergenes in the cases of Batesian mimicry in butterflies, distylous plants and sex chromosomes. For each of these systems, I outline the genetic evidence that led to the proposal that they involve multiple genes that interact during ‘complex adaptations’, and at which the mutations involved are not unconditionally advantageous, but show advantages that trade‐off against some disadvantages. I describe recent molecular genetic studies of these systems and questions they raise about the evolution of suppressed recombination. Nonrecombining regions of sex chromosomes have long been known, but it is not yet fully understood why recombination suppression repeatedly evolved in systems in distantly related taxa, but does not always evolve. Recent studies of distylous plants are tending to support the existence of recombination‐suppressed genome regions, which may include modest numbers of genes and resemble recently evolved sex‐linked regions. For Batesian mimicry, however, molecular genetic work in two butterfly species suggests a new supergene scenario, with a single gene mutating to produce initial adaptive phenotypes, perhaps followed by modifiers specifically refining and perfecting the new phenotype.

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“…subject to increased masculinizing selection. However, the avian Z and W chromosomes diverged in a stepwise process, and there is a considerable difference in the age of these strata (Wright et al 2012(Wright et al , 2014Wang et al 2014;Zhou et al 2014). Given the difference in age across these regions, we expected cumulative exposure to masculinizing selection to differ across the Z chromosome (Wright et al 2012).…”

Section: Regional Variation In Z-chromosome Masculinizationmentioning

confidence: 99%

“…Recombination between the Z and W ceased independently in Galliformes and Anseriformes for the youngest region of the sex chromosomes (Wright et al 2014), and we can therefore divide the Z into the old conserved region (regions corresponding to 43-80 Mb on the chicken Z chromosome) and young independently evolving portion (regions corresponding to 0-43 Mb on the chicken Z chromosome). We excluded the MHM region from this analysis.…”

Section: Regional Variation In Z-chromosome Masculinizationmentioning

confidence: 99%

Conservation of Regional Variation in Sex-Specific Sex Chromosome Regulation

Wright

Zimmer²,

Harrison³

et al. 2015

Genetics

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Regional variation in sex-specific gene regulation has been observed across sex chromosomes in a range of animals and is often a function of sex chromosome age. The avian Z chromosome exhibits substantial regional variation in sex-specific regulation, where older regions show elevated levels of male-biased expression. Distinct sex-specific regulation also has been observed across the male hypermethylated (MHM) region, which has been suggested to be a region of nascent dosage compensation. Intriguingly, MHM region regulatory features have not been observed in distantly related avian species despite the hypothesis that it is situated within the oldest region of the avian Z chromosome and is therefore orthologous across most birds. This situation contrasts with the conservation of other aspects of regional variation in gene expression observed on the avian sex chromosomes but could be the result of sampling bias. We sampled taxa across the Galloanserae, an avian clade spanning 90 million years, to test whether regional variation in sexspecific gene regulation across the Z chromosome is conserved. We show that the MHM region is conserved across a large portion of the avian phylogeny, together with other sex-specific regulatory features of the avian Z chromosome. Our results from multiple lines of evidence suggest that the sex-specific expression pattern of the MHM region is not consistent with nascent dosage compensation.KEYWORDS sex-biased gene expression; male hypermethylated region S EX chromosomes exhibit extensive sex-specific gene regulation in many animals, largely resulting from two independent forces. First, the reduced gene content on the sex-limited Y or W chromosome observed in many species (Bachtrog 2013) leads to a reduction in gene dose in the heterogametic sex for X-or Z-linked genes. Because gene expression is often a function of gene dose, this dosage effect (Zhang et al. 2013) means that many X-or Z-linked loci show differences in gene expression between males and females. Variation in gene dose is often thought to be detrimental, and different mechanisms of dosage compensation have evolved to address the differences in sex chromosome dose in some organisms (Mank 2013). Dosage compensation mechanisms in several organisms show extensive regional variation, with some regions exhibiting less complete compensation than other regions on the therian (Carrel and Willard 2005) and stickleback (Schultheiß et al. 2015) X chromosomes.Second, independent of gene dose differences, sex chromosomes are also inherited unequally between the sexes, leading to distinct evolutionary forces relative to the autosomes (Rice 1984;Charlesworth et al. 1987). In particular, conflicting selection on males and females results in unequal sex-specific selection pressures acting on the sex chromosomes. This, in turn, influences rates of sequence and expression evolution (Vicoso and Charlesworth 2009;Meisel and Connallon 2013). Older sex chromosome regions, where recombination between the Z-W orthologs was halted earlier...

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Independent Stratum Formation on the Avian Sex Chromosomes Reveals Inter‐chromosomal Gene Conversion and Predominance of Purifying Selection on the W Chromosome

Cited by 55 publications

References 99 publications

Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators

Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators

The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations

Conservation of Regional Variation in Sex-Specific Sex Chromosome Regulation

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