Genomic evidence reveals three sequential W-autosome fusions in Heliconius butterflies

Sex chromosomes are evolutionarily labile in many animals and sometimes fuse with autosomes, creating so-called neo-sex chromosomes. Fusions between sex chromosomes and autosomes have been proposed to reduce sexual conflict and to promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of such fusions across the tree of life. Here, we discovered multiple fusions leading to neo-sex chromosomes in the sara/sapho clade of the classical adaptive radiation of Heliconius butterflies. Heliconius butterflies generally have 21 chromosomes with very high synteny. However, the five species in the sapho subclade show large variation in chromosome number ranging from 21 to 60. We found that the W chromosome is fused with chromosome 4 in all of them. Two sister species pairs showed subsequent fusions between the W and chromosomes 9 or 14, respectively. These sequential fusions between autosomes and sex chromosomes make Heliconius butterflies an ideal system for studying the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our findings emphasize the capability of WGS technology to detect neo-sex chromosomes even when sex chromosomes are not explicitly assembled. Author SummaryFusions between sex chromosomes and autosomes are thought to have the potential to resolve sexual conflict and enhance local adaptation or reproductive isolation between species. Here, we discovered such fusions in Heliconius butterflies. Heliconius butterflies mostly have a very stable karyotype with 21 chromosomes and high synteny across species. However, the five species in the sapho subclade have up to 60 chromosomes, suggesting that they have undergone many chromosomal fissions. We document that in addition to the fissions, the sapho subclade also showed multiple fusions between the female-specific sex chromosome (W) and autosomes. We found a W-4 fusion shared by all five species and additional W fusions with chromosomes 9 and 14 shared by two species each. Even though in many sapho subclade species the autosomes have undergone fissions, the chromosomes fused with the W represent the full-length autosomes, as seen in other Heliconius species, suggesting that fusing to the W protected them from fissions. Our study reveals the power of short-read sequencing to discover neo-sex chromosomes and showcases Heliconius butterflies as a promising system for studying the causes and consequences of sex chromosome evolution.