Sex-biased gene content associates with sex chromosome turnover in Danaini butterflies

Sex chromosomes play an outsized role in adaptation and speciation, and
thus deserve particular attention in evolutionary genomics. In particular,
fusions between sex chromosomes and autosomes can produce neo-sex
chromosomes, which offer important insights into the evolutionary dynamics
of sex chromosomes. Here we investigate the evolutionary origin of the
previously reported Danaus neo-sex chromosome within the tribe Danaini. We
assembled and annotated genomes of Tirumala septentrionis (subtribe
Danaina), Ideopsis similis (Amaurina), Idea leuconoe (Euploeina), and
Lycorea halia (Itunina) and identified their Z-linked scaffolds. We found
that the Danaus neo-sex chromosome resulting from the fusion between a Z
chromosome and an autosome corresponding to the Melitaea cinxia chromosome
(McChr) 21 arose in a common ancestor of Danaina, Amaurina, and Euploina.
We also identified two additional fusions as the W chromosome further
fused with the synteny block McChr31 in I. similis and
independent fusion occurred between the ancestral Z chromosome and McChr12
in L. halia. We further tested a possible role of sexually
antagonistic selection in sex chromosome turnover by analyzing the genomic
distribution of sex-biased genes in I. leuconoe and L. halia. The
autosomes corresponding to McChr21 and McChr31 involved in the fusions are
significantly enriched in female- and male-biased genes, respectively,
which could have hypothetically facilitated fixation of the neo-sex
chromosomes. This suggests a role of sexual antagonism in sex chromosome
turnover in Lepidoptera. The neo-Z chromosomes of both I. leuconoe and L.
halia appear fully compensated in somatic tissues, but the extent of
dosage compensation for the ancestral Z is variable across tissues and
species.