Genomic structural variation in clownfish adaptive radiation

Abstract

Clownfishes are a complex of 28 species that rapidly diversified after acquiring mutualism with host sea anemones around 15 million years ago. The genomic mechanisms behind this radiation are only beginning to emerge, and structural variants (SVs) have received little attention. Previous phylogenomic studies suggested two large inversions on chromosome 18, but their distribution across the clownfish phylogeny and their potential effects have not been formally explored. SVs can disrupt gene function and regulation or alter gene dosage, and they have been shown to play a central role in adaptive evolution and diversification across many taxa. Here, we characterized SVs across the clownfish radiation using long-read PacBio sequencing, generating high-quality genome assemblies for sixteen species spanning the main lineages of the genus. We identified and catalogued nearly 130,000 SVs spanning close to 570 Mb. Short insertions and deletions were the most numerous, but large inversions accounted for most of the affected sequence. No SV was consistently associated with host specialization. We nevertheless confirmed a single inversion of approximately 17 Mb on chromosome 18, clarifying earlier reports of two separate rearrangements at this locus, and identified an additional inversion on chromosome 9 whose distribution suggests a history of hybridization. This study provides the first genome-wide characterization of structural variation in clownfishes, revealing extensive SVs despite the group's rapid and recent radiation. It also delivers new, high-quality genomic resources that will support future research into this iconic group of coral reef fishes and their adaptation to sea anemones.