Spatial Dynamics of Evolving Dosage Compensation in a Young Sex Chromosome System

Abstract

The loss of Y-linked genes during sex chromosome evolution creates a potentially deleterious low gene dosage in males. Recent studies have reported different strategies of dosage compensation. Unfortunately, most of these studies investigated taxa with comparatively old sex chromosome systems, which may limit insights into the evolution of dosage compensation and thus into the causes of different compensation strategies. Using deep RNA sequencing, we investigate differential expression patterns along the young XY chromosomes of threespine sticklebacks. Our strata-specific analyses provide new insights into the spatial patterns during the early stages of the evolution of dosage compensation. In particular, our results indicate systematic upregulation of male gene expression in stratum II, which in turn causes female hypertranscription in the same stratum. These findings are consistent with theoretical predictions that selection during early stages of sex chromosome evolution is stronger for a compensating upregulation in males than for the countercompensation of female hyperexpression. In contrast, no elevated gene expression is detectable in stratum I. We argue that strata-specific differences in compensating male gene expression may evolve in response to differences in the prevailing mechanism of Y chromosome degeneration.

Regulatory Architecture of Gene Expression Variation in the Threespine Stickleback Gasterosteus aculeatus

“…The stickleback chromosome 19 is a proto-sex chromosome (Peichel et al 2004; Roesti et al 2013; Schultheiß et al 2015), with a normally recombining pseudoautosomal domain (∼0–2.5 Mb), a nonrecombining domain in the male version (Stratum I, ∼2.5–12 Mb), and a domain largely absent in the male version (Stratum II, ∼12–20 Mb). For Stratum I, parental and offspring genotypes were inspected manually in order to identify the male-specific allele and this was recoded to a unique allele code (“9”) for the purposes of linkage map construction.…”

Dosage compensation of the sex chromosomes and autosomes

“…In sticklebacks recently evolved sex chromosomes allowed the definition of two main strata along the X, with the older strata showing evidence of upregulation in males and overexpression in females at least for a subset of genes [98]. Complete dosage compensation by upregulation of the male X chromosome evolved independently in Drosophila melanogaster and in a mosquito Anopheles stephensi [99], while in another insect, Heliconius butterfly, there is only partial dosage compensation [100].…”

Conservation of Regional Variation in Sex-Specific Sex Chromosome Regulation

“…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.…”

“…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.…”