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

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 to 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, in order to understand the evolution of dosage compensation.

性染色体剂量补偿（sex chromosome dosage compensation）会在异配性别中平衡同配性染色体与常染色体的表达水平，从而实现两性间性染色体表达量的均等。若剂量补偿不完全，则会引发表达失衡与性别偏向性基因表达。近期研究揭示了物种间剂量补偿模式既引人关注又存在多样性的特点：相较于XY型性别决定物种，ZW型性别决定物种普遍缺乏完全的剂量补偿。据此学界提出假说：ZW型物种或许无需完全的剂量补偿，或者完全剂量补偿会对其适合度产生负面影响。截至目前，仅有一项针对家蚕（Bombyx mori）的研究在ZW型物种中找到了完全剂量补偿的证据。本研究选取另一种蛾类——烟草天蛾（Manduca sexta），通过高通量测序技术对其雌雄成虫头部组织的基因表达谱进行了检测。结果显示，烟草天蛾的剂量补偿完全：雌雄个体的Z染色体平均表达水平完全一致。经过滤去除低表达量基因后，常染色体的平均表达水平与Z染色体平均表达水平高度相似，这表明烟草天蛾体内绝大多数基因都实现了完全剂量补偿。此外，该剂量补偿过程还伴随着与重要性别二态性性状相关的性别特异性基因表达。本研究认为，ZW型物种中的完全剂量补偿或许比此前认知的更为普遍，且这一过程可能与性选择等额外的选择进程相关联。未来应在系统发育框架下对更多ZW型及鳞翅目（Lepidoptera）物种展开研究，以阐明剂量补偿的演化机制。