Rapid turnover of sex chromosomes is associated with speciation in Neotropical armored catfish Harttia (Siluriformes, Loricariidae)

Abstract Background The Neotropical armored catfish genus Harttia is an exceptional model for studying sex chromosome evolution, as it harbors the highest diversity of multiple sex chromosome systems known among fishes. However, the evolutionary history of these systems and their contribution to lineage diversification remain unresolved. We generated genome-wide DArTseq data for 17 Harttia species to investigate the origins of sex chromosome turnover, reconstruct phylogenetic and biogeographic history, identify sex-linked markers, and test whether multiple sex chromosomes are associated with increased speciation. Results Genome-wide SNP analyses resolved three major Harttia clades and dated their diversification to the last 10 million years, coinciding with major Neotropical drainage rearrangements. We identified 443 candidate sex-linked markers that suggest independent origins for the X₁X₂Y and XY₁Y₂ multiple sex chromosome systems. Ancestral chromosome-number reconstruction supported an ancestral karyotype of 2n = 58, while integration of candidate sex-linked markers with previous cytogenetic evidence is consistent with an ancestral homomorphic XY system followed by independent chromosome rearrangements generating multiple sex chromosomes in distinct lineages. State-dependent diversification analyses revealed significantly higher speciation rates in clades carrying multiple sex chromosomes than in those with simple systems, suggesting a close association between rapid sex chromosome turnover and lineage diversification. Conclusions Our results provide the first genome-wide evolutionary framework for Harttia , suggesting that multiple sex chromosome systems may be associated with elevated diversification in some Harttia lineages, while highlighting the need for broader genomic and taxonomic sampling to test this association. These findings identify Harttia as a powerful model for investigating how sex chromosome turnover, chromosome evolution, and landscape history jointly shape biodiversity.