The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W

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.

Fig. 1

Evidence and models for the secondary origin of the W chromosome. a Presence/absence of the W chromosome across a simplified phylogeny of Lepidoptera. The table shows, for each family, the total number of chromosomes; the presence (yes), absence (no) or non-determination (n.d.) of sex chromatin; as well as the cytogenetic confirmation of the presence of the W chromosome (adapted from Dalíková et al. 15). In Hepialidae, only some species, which did not include T. sylvina, were cytogenetically investigated to assess the presence/absence of the W (asterisk). Dotted lines represent families that are not investigated in our study, while gray circles show the five studied species. b Hypotheses for the secondary acquisition of the W chromosome. The ancestral Z0 female karyotype is represented by the Z chromosome (in red) and two pairs of autosomes (A1 and A2, in blue). In the two canonical models (Z-autosome fusion and sex chromosome turnover), the new sex chromosomes derived from a standard pair of autosomes (A1). In the non-canonical model, the W chromosome has a non-autosomal origin (in black), e.g., the recruitment of a B chromosome. The blue dotted lines represent the secondary degradation of the neo-W chromosome

Fig. 2

The Z chromosome of B. mori is homologous to that of the other species. Cameraria ohridella has additionally acquired a neo-Z chromosome (Chr. 18). For each species, scaffolds were assigned to one of the B. mori chromosomes based on their gene content. The Log2 of the female to male coverage ratio of each chromosome is shown for a C. ohridella, b N. degeerella, and c T. sylvina. Scaffolds mapping to the B. mori Z chromosome, and the neo-Z chromosome of C. ohridella, are in red, those mapping to the autosomes are in blue

Fig. 3

Homology between the Z chromosome of B. mori and that of the other species. For each species, scaffolds mapping to the Z chromosome of B. mori (Chr. 1) have been classified as Z-linked (in red), autosomal (in blue), or unclassified (in gray). The Log2 of the female to male coverage ratio along the B. mori Z chromosome (Chr. 1) is shown for a C. ohridella, b N. degeerella, and c T. sylvina. Dashed lines are moving average based on sliding windows of 10 scaffolds

Fig. 4

Gene movement onto and off the Z chromosome. a Lenient classification (4132 genes classified). b Stringent classification (3189 genes classified). The phylogenetic tree is adapted from Regier et al.. Red circles show the number of genes present on the ancestral Z chromosome. Arrows indicate the number of genes that move onto (up red arrows) or off (down blue arrows) the Z chromosome in each lineage after the split with T. sylvina. The top row indicates the total number of genes classified as Z-linked (Z) or autosomal (A) in each species

Fig. 5

Evidence of a W chromosome in C. ohridella but not in N. degeerella. Amplification patterns of genomic DNA from three females and three males are shown for two W-candidates, and for two autosomal control genes in a C. ohridella and b N. degeerella. The molecular size marker is indicated on the left (100 bp ladder). Results for all W-candidates are shown in Supplementary Fig. 5