Three sequential sex chromosome – autosome fusions inHeliconiusbutterflies

Abstract

AbstractSex chromosomes are evolutionarily labile in many animals, and fusion with an autosome is one of the mechanisms by which they can evolve. Sex chromosome-autosome (SA) fusions can reduce sexual conflict and promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of SA fusions in multiple vertebrates and in some invertebrates such as Lepidoptera. Here, we discovered multiple SA fusions in thesara/saphoclade of the classical adaptive radiation ofHeliconiusbutterflies. While the vast majority ofHeliconiusspecies have 21 chromosomes, species of the particularly rapidly diversifyingsaphoclade have up to 60 chromosomes. We found a sex chromosome fusion with chromosome 4 at the base of thesaphoclade and two additional sex chromosome fusions, each shared by two species. These sequential fusions between autosomes and sex chromosomes make theHeliconius saphoclade an ideal system to study the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our study adds to a small but growing number of examples in butterflies with sex chromosome fusions that will help to unravel the importance of such rearrangements in the evolution of Lepidoptera and eukaryotes in general.Author SummaryChromosome number and structure are fundamental characteristics of a species. However, chromosomal rearrangements can occur spontaneously within a species, which can have significant consequences for recombination, segregation, speciation, and adaptation. Despite the importance of chromosomal rearrangements in evolution, we still have limited knowledge of the drivers and consequences of chromosomal fusions and fissions in natural populations, especially in adaptive radiations such asHeliconiusbutterflies. For the first time, we document chromosomal fusions between sex chromosomes and autosomes inHeliconius, particularly in species from thesara/saphoclade. Our research provides evidence for sex-autosome fusions involving autosomes 4, 9, and 14. All of these fusions seem to be associated with speciation events in this clade, with the sex-autosome 4 fusion being the oldest one. Although we do not yet understand the role or evolutionary consequences of these fusions, our study shows that chromosomal structure can evolve rapidly within a clade and generate chromosomal diversity. Overall, our findings contribute to a better understanding of chromosome evolution in highly diverse species.