Analyses Of Sex Chromosome Dosage Compensation In The Codling Moth, Cydia Pomonella (Lepidoptera:Tortricidae) Yield Insights Into Sex Chromosome Evolution In Lepidoptera

Abstract

Dosage problems of sex-linked genes accompany degenerating sex chromosomes, which animals deal with differently. Species with male heterogametic sex chromosomes (XX/XY) employ different chromosome-wide mechanisms to equalize X-linked gene expression between sexes (X~XX compensation: X [ALMOST EQUAL TO] XX). Lepidopterans (moths and butterflies) have female heterogametic sex chromosomes (ZZ/ZW). Recognition of dosage compensation is controversial in this insect order due to differences in sequencing platforms, methods of analyses and tissues sampled. Among the other ZZ/ZW taxa examined so far, however, it is unanimously reported that overall Z-linked gene expression is reduced in females compared to males or the autosomes (Z < ZZ [ALMOST EQUAL TO] AA), reflection of lack of global dosage compensation. In this study, I assessed dosage compensation in the codling moth Cydia pomonella (Tortricidea), a basal moth species compared to the other lepidopterans that have been examined for dosage compensation. C. pomonella has a Z chromosomal segment (neo-Z) that arose from an autosome translocating to the ancestral Z chromosome (ancl-Z). I assembled the C. pomonella transcriptome de novo from RNAseq data and inferred the chromosome locations of identified transcripts by comparison to the Bombyx mori reference genome. These data showed that in C. pomonella overall Z-linked gene expression was balanced between sexes but reduced relative to that of the autosomes (Z [ALMOST EQUAL TO] ZZ < AA). The Z~ZZ compensation was complete on both the ancl-Z and neo-Z chromosomes in the head and midgut, suggesting the existence of a global compensation mechanism. The extent of Z~A compensation varied among tissues, being least in the ovary and most in male reproductive tissues. Comparison of the C. pomonella transcriptome with those of other Lepidopteran species with conserved karyotypes confirmed both complete Z~ZZ compensation and imperfect Z~A compensation in this species. Further, I found that the skewed gene content of the Z chromosome did not confound the analysis of dosage compensation. The pattern of dosage compensation in C. pomonella is consistent with that described for several other Lepidopteran species. However, a different pattern reported in Plodia interpunctella may reflect the use of whole body transcriptomes or problems with data processing in that study. The dosage compensation pattern in Lepidoptera mirrors that in mammals and suggests the inactivation of one Z chromosome copy in male moths. This is the first report of dosage compensation analysis of a neo-sex chromosome in a female heterogametic (ZZ/ZW) species, and presents the Lepidoptera as a unique taxon to broaden our understanding of dosage compensation and sex chromosome evolution.