Convergent patterns of sex chromosome dosage compensation between lepidopteran species (WZ/ZZ) and eutherian mammals (XX/XY): insights from a moth neo-Z chromosome

In contrast to XX/XY species, Z-linked expression is overall reduced in female WZ/ZZ species compared to males or the autosomal expression. This pattern (Z<ZZ{approx}AA) has been consistently reported in all the WZ/ZZ taxa examined so far, with the singular exception of the insect order of Lepidoptera (moths and butterflies). However, conflicting results linger in this taxon due to discrepancies in data analyses and tissues sampled. To address this issue, we analyzed dosage compensation in the codling moth Cydia pomonella (Tortricidae) using tissues that represent different levels of sexual divergence. C. pomonella is the most basal lepidopteran species yet examined for dosage compensation and has a neo-Z chromosome resulting from an ancient Z:autosome translocation. We based our analyses on RNAseq and de novo transcriptome data from C. pomonella, as well as scrutiny into investigations of other lepidopteran species. Our evidence supports that the lepidopterans share a pattern (Z {approx} ZZ < AA) of dosage compensation that mirrors the eutherian mammals (X {approx} XX < AA). In particular, reproductive tissues appear to be exempt from dosage compensation, which helps explain the incongruence in prior reports. Furthermore, C. pomonella ancestral-Z segment exhibited a greater expression reduction than genes on the neo-Z segment, which intriguingly also reflects the differential up-regulation between the ancestral and newly-acquired X-linked genes in mammals. The insect order of Lepidoptera challenges both the classic theories regarding evolution of sex chromosome dosage compensation and the emerging view on dosage compensations association with sexual heterogamety.