Abstract
Moths and butterflies (Lepidoptera) usually have a pair of differentiated WZ sex chromosomes. However, in most lineages outside of the division Ditrysia, as well as in the sister order Trichoptera, females lack a W chromosome. The W is therefore thought to have been acquired secondarily. Here we compare the genomes of three Lepidoptera species (one Dytrisia and two non-Dytrisia) to test three models accounting for the origin of the W: (1) a Z-autosome fusion; (2) a sex chromosome turnover; and (3) a non-canonical mechanism (e.g., through the recruitment of a B chromosome). We show that the gene content of the Z is highly conserved across Lepidoptera (rejecting a sex chromosome turnover) and that very few genes moved onto the Z in the common ancestor of the Ditrysia (arguing against a Z-autosome fusion). Our comparative genomics analysis therefore supports the secondary acquisition of the Lepidoptera W by a non-canonical mechanism, and it confirms the extreme stability of well-differentiated sex chromosomes.
Highlights
Moths and butterflies (Lepidoptera) usually have a pair of differentiated WZ sex chromosomes
Male and female DNA reads were mapped separately to the assemblies using Bowtie[2], and genomic coverage was estimated with SOAPcoverage
Our comparative genomic analysis demonstrates the conservation of the Z chromosome over 140 Myr of Lepidoptera evolution[24] and further supports a shared ancestry of the Lepidoptera and Trichoptera Z chromosomes (Supplementary Fig. 3)
Summary
Moths and butterflies (Lepidoptera) usually have a pair of differentiated WZ sex chromosomes. Under the canonical model, such differentiated sex chromosomes initially arise from standard pairs of autosomes: after acquiring a sex-determining gene, newly formed Y (or W) chromosomes accumulate sexually antagonistic mutations that are favorable to the sex they are found in (reviewed in Wright et al.[2]). The presence of such mutations eventually favours the loss of recombination between the sex chromosomes, in order to achieve full linkage between sex and alleles with sex-specific benefits, and sets in motion the degeneration of the sex-specific chromosome[2]. The absence of such sex chromatin bodies in other independent nonditrysian lineages[11] has led to the suggestion that the Z0 system is ancestral and that the W chromosome was acquired secondarily either in the ancestor of all Ditrysia and Tischerioidea[11,12,13,14], or early in the evolution of the Ditrysia[15] (Fig. 1a)
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