Genomic evidence reveals three W-autosome fusions in Heliconius butterflies

PLoS Genet. 2024 Jul 18;20(7):e1011318. doi: 10.1371/journal.pgen.1011318. eCollection 2024 Jul.

Abstract

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 sapho subclade of the classical adaptive radiation of Heliconius butterflies. Heliconius butterflies generally have 21 chromosomes with very high synteny. However, the five Heliconius species in the sapho subclade show large variation in chromosome number ranging from 21 to 60. We find that the W chromosome is fused with chromosome 4 in all of them. Two sister species pairs show subsequent fusions between the W and chromosomes 9 or 14, respectively. These 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 short-read resequencing to detect genomic signatures of fusion events between sex chromosomes and autosomes even when sex chromosomes are not explicitly assembled.

MeSH terms

  • Animals
  • Butterflies* / genetics
  • Chromosomes, Insect / genetics
  • Evolution, Molecular*
  • Female
  • Genome, Insect
  • Genomics / methods
  • Male
  • Phylogeny
  • Sex Chromosomes* / genetics
  • Synteny

Grants and funding

This work was supported by the Universidad del Rosario (https://urosario.edu.co/) (BigGrant IV-FGD005 and Fondos Concursables IV-FPD004 to CS and CP); Colombian Ministry of science, technology and innovation (https://minciencias.gov.co/) (MinCiencias – doctoral scholarship 727 to NRM); Branco Weiss – Society in Science fellowship, Royal Society University Research Fellowship and Wellcome Trust award (https://brancoweissfellowship.org/, https://royalsociety.org/ and https://wellcome.org/) (URF\R1\221041 and 220540/Z/20/A to JIM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.