Academic journal article Genetics

Trade-Off between Selection for Dosage Compensation and Masculinization on the Avian Z Chromosome

Academic journal article Genetics

Trade-Off between Selection for Dosage Compensation and Masculinization on the Avian Z Chromosome

Article excerpt

ABSTRACT Following the suppression of recombination, gene expression levels decline on the sex-limited chromosome, and this can lead to selection for dosage compensation in the heterogametic sex to rebalance average expression from the X or Z chromosome with average autosomal expression. At the same time, due to their unequal pattern of inheritance in males and females, the sex chromosomes are subject to unbalanced sex-specific selection, which contributes to a nonrandom distribution of sex-biased genes compared to the remainder of the genome. These two forces act against each other, and the relative importance of each is currently unclear. The Gallus gallus Z chromosome provides a useful opportunity to study the importance and trade-offs between sex-specific selection and dosage compensation in shaping the evolution of the genome as it shows incomplete dosage compensation and is also present twice as often in males than females, and therefore predicted to be enriched for male-biased genes. Here, we refine our understanding of the evolution of the avian Z chromosome, and show that multiple strata formed across the chromosome over ~130 million years. We then use this evolutionary history to examine the relative strength of selection for sex chromosome dosage compensation vs. the cumulative effects of masculinizing selection on gene expression. We find that male-biased expression increases over time, indicating that selection for dosage compensation is relatively less important than masculinizing selection in shaping Z chromosome gene expression.

MALES and females of the same species are subject to distinct selective forces, often resulting in contradictory sex-specific selection pressures acting on a given locus. These selective forces have been shown to affect large portions of the genome (Connallon et al. 2010) and can place a significant genetic and evolutionary burden on a species (Chippindale et al. 2001; Arnqvist and Rowe 2005; Morrow et al. 2008). At the genetic level, sexually antagonistic selection pressures are thought to contribute to gene expression differences observed between the sexes in many species (Rice 1984; Connallon and Knowles 2005; Ellegren and Parsch 2007).

The effect of sex-specific selection is particularly evident on the sex chromosomes, where the unbalanced pattern of inheritance creates uneven sex-specific selection pressures (Rice 1984; Charlesworth et al. 1987; Connallon and Clark 2010). Consequentially, the sex chromosomes are a hotspot of intralocus sexual conflict within the genome (Mank 2009; Innocenti and Morrow 2010), and unequal sex-specific selection is predicted to have contributed to the complex pattern of sex-biased gene distribution observed across the sex chromosomes of many animals (Parisi et al. 2003; Khil et al. 2004; Vicoso and Charlesworth 2006; Sturgill et al. 2007; Zhang et al. 2010a,b; Chen et al. 2011). Indeed, the avian Z chromosome exhibits a pervasive pattern of male-biased gene expression, which could be interpreted in the light of masculinizing selection for dominant male-benefit genes (Rice 1984; Ellegren et al. 2007; Itoh et al. 2007).

At the same time, sex chromosomes experience changes in gene dose. Due to lack of recombination with their homologs, Y and W chromosome gene activity slowly degenerates by neutral processes (Charlesworth 1996) and the buildup of nonsynonymous and nonsense mutations as well as small indels (Zhou and Bachtrog 2012), where the rate of decay declines with the number of functionally constrained loci (Bachtrog 2008). Gene expression loss shows a range of dominance (Agrawal and Whitlock 2011), and for some genes, loss-of-function mutations on the W or Y chromosome will cause negative fitness effects (Charlesworth 1978).

The resulting loss of gene activity in the heterogametic sex and thus unbalanced gene dose with the autosomes is predicted to be costly, especially for X- or Z-linked genes that interact with autosomal genes in large protein complexes (Pessia et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.