Getting a Full Dose? Reconsidering Sex Chromosome Dosage Compensation in the Silkworm, Bombyx mori

Abstract

Dosage compensation—equalizing gene expression levels in response to differences in gene dose or copy number—is classically considered to play a critical role in the evolution of heteromorphic sex chromosomes. As the X and Y diverge through degradation and gene loss on the Y (or the W in female-heterogametic ZW taxa), it is expected that dosage compensation will evolve to correct for sex-specific differences in gene dose. Although this is observed in some organisms, recent genome-wide expression studies in other taxa have revealed striking exceptions. In particular, reports that both birds and the silkworm moth (Bombyx mori) lack dosage compensation have spurred speculation that this is the rule for all female-heterogametic taxa. Here, we revisit the issue of dosage compensation in silkworm by replicating and extending the previous analysis. Contrary to previous reports, our efforts reveal a pattern typically associated with dosage compensated taxa: the global male:female expression ratio does not differ between the Z and autosomes. We believe the previous report of unequal male:female ratios on the Z reflects artifacts of microarray normalization in conjunction with not testing a major assumption that the male:female global expression ratio was unbiased for autosomal loci. However, we also find that the global Z chromosome expression is significantly reduced relative to autosomes, a pattern not expected in dosage compensated taxa. This combination of male:female parity with an overall reduction in expression for sex-linked loci is not consistent with the prevailing evolutionary theory of sex chromosome evolution and dosage compensation.

Sex chromosome dosage compensation inHeliconiusbutterflies: global yet still incomplete?

“…These patterns are consistent with our hypothesis of highly expressed testes genes generating a pattern of male overexpression in the top quartile. Furthermore, this pattern would be exacerbated on the Z chromosome due to the overrepresentation of male-biased genes on the Z, as observed here (see below) and also reported in B. mori (Arunkumar et al 2009;Walters and Hardcastle 2011). Finally, we note there is additional experimental evidence for a global sex chromosome dosage mechanism that downregulates male Z expression, at least in B. mori.…”

“…This process should also result, indirectly, in balanced gene expression between the sexes for the X/Z. One important working assumption in this framework is that average expression is approximately equal across autosomes, therefore "complete" dosage compensation should yield X:A (or Z:A) expression ratios of approximately 1 in both sexes (Nguyen and Disteche 2006;Mank 2009Mank , 2013Vicoso and Bachtrog 2011;Walters and Hardcastle 2011;Smith et al 2014).…”

Sex chromosome evolution in moths and butterflies

“…The results were confirmed in most genes of a wider, microarray-based investigation of transcription levels of 579 Z-linked genes in B. mori: Hence, it appears that Lepidoptera do not have a chromosome-wide dosage compensation mechanism (Zha et al 2009). In a new microarray study, Walters and Hardcastle (2011) found a 1:1 ratio of Z chromosomal transcript levels between females and males relative to autosomal gene expression. From these data, it seems that there is dosage compensation in B. mori.…”

“…For unknown reasons, the Z chromosome carries an overproportionate number of genes solely expressed in the testis (Arunkumar et al 2009;Walters and Hardcastle 2011).…”

Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome

“…Partial Z chromosome dosage compensation has also been observed in silkworm (29,30) and in the parasite Schistosoma mansoni (31). Studies on the platypus indicate incomplete X chromosome dosage compensation in monotremes (32,33).…”