Complete dosage compensation and sex-biased gene expression in the moth Manduca sexta

Abstract

Sex chromosome dosage compensation balances homogametic sex chromosome expression with autosomal expression in the heterogametic sex, leading to sex chromosome expression parity between the sexes. If compensation is incomplete, this can lead to expression imbalance and sex-biased gene expression. Recent work has uncovered an intriguing and variable pattern of dosage compensation across species that includes a lack of complete dosage compensation in ZW species compared with XY species. This has led to the hypothesis that ZW species do not require complete compensation or that complete compensation would negatively affect their fitness. To date, only one study, a study of the moth Bombyx mori, has discovered evidence for complete dosage compensation in a ZW species. We examined another moth species, Manduca sexta, using high-throughput sequencing to survey gene expression in the head tissue of males and females. We found dosage compensation to be complete in M. sexta with average expression between the Z chromosome in males and females being equal. When genes expressed at very low levels are removed by filtering, we found that average autosome expression was highly similar to average Z expression, suggesting that the majority of genes in M. sexta are completely dosage compensated. Further, this compensation was accompanied by sex-specific gene expression associated with important sexually dimorphic traits. We suggest that complete dosage compensation in ZW species might be more common than previously appreciated and linked to additional selective processes, such as sexual selection. More ZW and lepidopteran species should now be examined in a phylogenetic framework, to understand the evolution of dosage compensation.

Keywords: Lepidoptera; dosage compensation; mushroom body; olfaction; phototransduction; sex-biased gene expression.

Fig. 1.—

Histogram showing log₂ male:female ratio of expression level (FPKM) for Manduca sexta contigs located on the Z chromosome (red) and the autosomes (blue; a), and all contigs regardless of physical location (b).

Fig. 2.—

Average Z-linked and autosomal contig expression levels (FPKM) across four replicate males and females using the log₂ outlier removal method of filtering (a) and removal of contigs with less than 4 FPKM (b). Black lines are the median of the FPKM distribution across contigs, boxes show the interquartile range, whiskers extend to 1.5 × the interquartile range and notches approximate the 95% confidence intervals of the medians. Overlapping notches are evidence for the similarity of median values.

Fig. 3.—

Heatmap of significantly DE genes (FDR < 0.05) plotted using log₂ counts per million (log CPM) per gene for each Manduca sexta library (males 1–4 and females 1–4, as labeled; a). Color bar legend indicates the degree of log CPM change between males and females. (b) Physical locations of sex-biased genes determined using 1:1 orthologs in Bombyx mori. Chromosome numbers are shown, with the Z chromosome being chromosome 1, as indicated. The size of each chromosome segment in the pie chart represents the relative abundance of sex-biased genes, normalized to chromosome size.

Fig. 4.—

Putative models of X/Z chromosomal dosage compensation for representative XY and ZW species. Chromosomes represent the X/Z (large chromosomes) and Y/W (small chromosomes) across XY and ZW species, for males and females, and a brief summary of the putative mechanism is provided (if known; grey boxes). See Introduction for details. Blue chromosomes represent normal gene expression levels across chromosomes, red chromosomes represent upregulated gene expression, and black chromosomes inactivated chromosomal expression. References are as follows: ¹Johnston et al. (2008); ²Straub et al. (2005); ³Deakin et al. (2009); ⁴Julien et al. (2012); ⁵Prince et al. (2010); ⁶Current study; ⁷Walters and Hardcastle (2011); ⁸Harrison et al. (2012); ⁹Itoh et al. (2010); ¹⁰Adolfsson and Ellegren (2013).