A butterfly pan-genome reveals a large amount of structural variation underlies the evolution of chromatin accessibility

Abstract

Despite insertions and deletions being the most common structural variants (SVs) found across genomes, not much is known about how much these SVs vary within populations and between closely related species, nor their significance in evolution. To address these questions, we characterized the evolution of indel SVs using genome assemblies of three closely related Heliconius butterfly species. Over the relatively short evolutionary timescales investigated, up to 18.0% of the genome was composed of indels between two haplotypes of an individual H. charithonia butterfly and up to 62.7% included lineage-specific SVs between the genomes of the most distant species (11 Mya). Lineage-specific sequences were mostly characterized as transposable elements (TEs) inserted at random throughout the genome and their overall distribution was similarly affected by linked selection as single nucleotide substitutions. Using chromatin accessibility profiles (i.e., ATAC-seq) of head tissue in caterpillars to identify sequences with potential cis-regulatory function, we found that out of the 31,066 identified differences in chromatin accessibility between species, 30.4% were within lineage-specific SVs and 9.4% were characterized as TE insertions. These TE insertions were localized closer to gene transcription start sites than expected at random and were enriched for several transcription factor binding site candidates with known function in neuron development in Drosophila. We also identified 24 TE insertions with head-specific chromatin accessibility. Our results show high rates of structural genome evolution that were previously overlooked in comparative genomic studies and suggest a high potential for structural variation to serve as raw material for adaptive evolution.

Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

“…S24). This suggests that selection may have favoured a reduction in TEs in intergenic regions, perhaps to avoid the disruption of regulatory elements (15), consistent with TEs largely accumulating in the tails of chromosomes (16). Although intron size varies significantly, the rate of gain/loss of introns, and the intron retention from the MRCA of Nymphalids, shows a relatively stable dynamic over the last 50 Mya in Heliconiinae, with no significant shift among species, and ~7% of ancestral intron sites retained across species (Fig.…”

Chromosomal conservatism vs chromosomal megaevolution: enigma of karyotypic evolution in Lepidoptera

“…A high level of macrosynteny does not indicate a complete absence of structural evolution of chromosomes. For several species, the presence of a large number of microarrangements (insertions and deletions) separating homologous chromosomes has been shown (d’Alençon et al, 2010; Ruggieri et al, 2022). Our data also show that against the background of conservation of macrosyntheny (gene order), the compared species differ greatly in the length of DNA repeats.…”

Recent advances in crustacean genomics and their potential application in aquaculture

“…In turn, this facilitates the elucidation of genotype–phenotype associations and establishes a solid foundation for future biological studies and genetic breeding 179,180 . Pan‐genome studies have been widely conducted in microorganisms, plants, and some animals (e.g., vertebrates, molluscs and insects) but not in crustaceans 181–187 . 3D genomics is an approach for studying the spatial and temporal architecture of a genome, which helps us understand how chromatin is organized within the nucleus and how this 3D architecture influences gene regulation, cell fate and evolution 188 .…”