Evolution of Sex Chromosome Dosage Compensation in Animals: A Beautiful Theory, Undermined by Facts and Bedeviled by Details

Gu, Liuqi; Walters, James R.

doi:10.1093/gbe/evx154

Cited by 123 publications

(228 citation statements)

References 141 publications

(284 reference statements)

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“…Heliconius males, expression of Z genes is reduced below autosomal levels, but this dosage compensation mechanism is imperfect, with males showing increased expression relative to females on Z chromosome genes (Walters et al, 2015). However, the apparent incomplete dosage compensation could be a consequence of an uneven distribution of sex-biased genes on sex chromosomes (Gu & Walters, 2017, Huylmans, Macon, & Vicoso, 2017. Regardless, when we compare rates of divergence and adaptation for genes with sex-biased expression, the expectations of fast-Z evolution are not clearly met.…”

Section: Discussionmentioning

confidence: 99%

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Pinharanda

Rousselle

Martin

et al. 2019

J of Evolutionary Biology

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Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex‐ and tissue‐specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male‐biased than female‐biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic‐specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast‐Z effect where hemizygosity influences the rate of adaptive substitutions.

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Section: Discussionmentioning

confidence: 99%

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Pinharanda

Rousselle

Martin

et al. 2019

J of Evolutionary Biology

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“…Finally, the rate of turnover of XY versus ZW chromosomes is predicted to differ in light of mutation load. First, the evolution of complete dosage compensation, a mechanism that compensates for the degeneration and loss of expression of the W and Y chromosomes (Gu & Walters, ; Mank, ), is thought to reduce the power of purifying selection to maintain gene activity on these chromosomes (Engelstädter, ; Wright et al, ). Dosage compensation mechanisms are more frequently observed on XY relative to ZW chromosomes in the species studied so far (Gu & Walters, ; Mullon et al, ; Tables –S3), potentially leading to faster rates of Y chromosome decay.…”

Section: Future Directions and Perspectivesmentioning

confidence: 99%

“…First, the evolution of complete dosage compensation, a mechanism that compensates for the degeneration and loss of expression of the W and Y chromosomes (Gu & Walters, ; Mank, ), is thought to reduce the power of purifying selection to maintain gene activity on these chromosomes (Engelstädter, ; Wright et al, ). Dosage compensation mechanisms are more frequently observed on XY relative to ZW chromosomes in the species studied so far (Gu & Walters, ; Mullon et al, ; Tables –S3), potentially leading to faster rates of Y chromosome decay. However, there have been several recent counter‐examples to this trend (Hale, McKinney, Thrower, & Nichols, ; Huylmans et al, ), and as more sex chromosomes are identified it will be possible to test whether there is indeed a consistent relationship between dosage compensation status and sex chromosome system.…”

Section: Future Directions and Perspectivesmentioning

confidence: 99%

Section: Accumulation Of Deleterious Mutationsmentioning

confidence: 99%

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How to identify sex chromosomes and their turnover

et al. 2019

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Although sex is a fundamental component of eukaryotic reproduction, the genetic systems that control sex determination are highly variable. In many organisms the presence of sex chromosomes is associated with female or male development. Although certain groups possess stable and conserved sex chromosomes, others exhibit rapid sex chromosome evolution, including transitions between male and female heterogamety, and turnover in the chromosome pair recruited to determine sex. These turnover events have important consequences for multiple facets of evolution, as sex chromosomes are predicted to play a central role in adaptation, sexual dimorphism, and speciation. However, our understanding of the processes driving the formation and turnover of sex chromosome systems is limited, in part because we lack a complete understanding of interspecific variation in the mechanisms by which sex is determined. New bioinformatic methods are making it possible to identify and characterize sex chromosomes in a diverse array of non‐model species, rapidly filling in the numerous gaps in our knowledge of sex chromosome systems across the tree of life. In turn, this growing data set is facilitating and fueling efforts to address many of the unanswered questions in sex chromosome evolution. Here, we synthesize the available bioinformatic approaches to produce a guide for characterizing sex chromosome system and identity simultaneously across clades of organisms. Furthermore, we survey our current understanding of the processes driving sex chromosome turnover, and highlight important avenues for future research.

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“…As Ohno noted [1], ‘The so-called sex-linked genes are nothing more than the original Mendelian genes which were there when the X or the Z was an ordinary chromosome’. These ‘ordinary’ genes are under strong developmental constraint to maintain expression levels between males and females through dosage compensation [reviewed in 2], leading to the remarkable conservation of X chromosome gene content across placental mammals [3], known as Ohno’s law [see also 4]. But sex-linked genes are often more than just ordinary genes.…”

Section: Constraint and Conflict In Sex Chromosome Evolutionmentioning

confidence: 99%

Spermatogenesis and the Evolution of Mammalian Sex Chromosomes

2018

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Developmental constraint and sexual conflict shape the evolution of heteromorphic sex chromosomes. These contrasting forces are perhaps strongest during spermatogenesis in species with XY males. In this review, we consider how the unique regulatory environment and selective pressures of spermatogenesis interact to impact sex chromosome evolution in mammals. We explore how each developmental phase of spermatogenesis influences sex chromosome gene content, structure, and rate of molecular evolution, and how these attributes may contribute to speciation. We argue that a developmental context is fundamental to understanding sex chromosome evolution and that an evolutionary perspective can shed new light on our understanding of sperm development.

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Evolution of Sex Chromosome Dosage Compensation in Animals: A Beautiful Theory, Undermined by Facts and Bedeviled by Details

Cited by 123 publications

References 141 publications

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

How to identify sex chromosomes and their turnover

Spermatogenesis and the Evolution of Mammalian Sex Chromosomes

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