Pattern of Sex Chromosome Dosage Compensation in Lepidoptera: Insights from a Fused Moth Z Chromosome

In male heterogametic species (XX/XY), the expression of X genes is balanced chromosome wide between sexes so that X (male) = XX (female). In contrast, for female heterogametic species (ZZ/ZW), has been unanimously reported among all ZZ/ZW taxa investigated so far that majority of Z genes are left uncompensated, resulting in reduced overall female Z expression compared to males (Z < ZZ). However, little is known regarding another ZZ/ZW taxon, the Lepidoptera (moth and butterflies). We assessed dosage compensation in the codling moth C. pomonella, which has a Z chromosome fused between an ancestral Z chromosome (old-Z segment) and an autosome (neo-Z segment). First, we compared overall expression of Z linked and autosomal genes between sexes based on de novo assembled transcriptome from mRNA sequencing. We further confirmed this pattern through comparative trancriptome approach, which compared the expression of genes residing on the ‘neo-Z’ segment with their autosomal orthologs present in two other Lepidoptera species. Last, we determined C. pomonella tissue specific genes by identifying differential expression using edgeR and then calculated proportion of tissue specific genes on each chromosome. We concluded that in C. pomonella adult tissues except for testis, Z chromosome expression is reduced relative to autosomes but without sex disparity (Z = ZZ): a unique pattern so far reported among all ZZ/ZW taxa investigated. Although Z chromosome is enriched with highly expressed testis specific genes, removing these genes however, do not change the dosage compensation pattern observed. Therefore, we suggest that the male Z chromosome(s) may be inactivated or suppressed in soma while restored in male germline, a process rather intriguingly analogous to XX/XY mammals.