From Adam’s rib: the Siberian moth’s female W chromosome is derived from its Z counterpart

Abstract Most lepidopteran species have a WZ/ZZ sex chromosome system, suggesting a common origin. However, the exceptional variability of W chromosomes supports their multiple independent origins. Here, we investigated the genome of the recently formed species, Dendrolimus sibiricus, which is one of the most devastating pests of the boreal forests in Northern Asia. We found that its karyotype consists of 30 pairs of chromosomes and follows the WZ/ZZ sex chromosome system. We produced a chromosome-scale assembly of its female genome and identified the sequences of both sex chromosomes. With the exception of the W chromosome, the D. sibiricus genome displays a very high degree of synteny with genomes of other Dendrolimus representatives. The non-conserved W chromosome is composed entirely of recently acquired sequences, mainly young genomic repeats and a few unique loci derived from subtelomeric regions of the same species’ Z chromosome as well as from the genome of the endosymbiotic Wolbachia bacterium. It shares no common ancestral sequences with the W chromosomes of two related species, D. tabulaeformis and Lasiocampa quercus. They, in turn, display a similar organization relative to the W of D. sibiricus, including Z-derived loci. The W of D. tabulaeformis also contained multiple fragments of the mitochondrial genome, as seen in classical B chromosomes. We conclude that W chromosomes arose from their Z counterparts recently and independently in these three species. We propose that this mechanism may be a common feature of lepidopteran evolution, counteracting the inevitable degeneration of a non-recombining chromosome through its repeated, complete turnover.