Rapid turnover of sex chromosomes likely drives speciation in Neotropical armored catfish Harttia (Siluriformes, Loricariidae)

The genus Harttia represents an important repository of multiple sex chromosomes, as they are found in more than a quarter of its valid species, exhibiting distinct degrees of heteromorphism. However, little is known about the evolution of these systems from a molecular perspective. In this study, we generated DArTseq data for 17 species of Harttia and one outgroup species ( Farlowella sp.) to investigate the genomic architecture underlying sex chromosome evolution in this highly dynamic genus. The time-calibrated phylogeny based on 1,381 SNPs revealed three well-supported clades, with divergence between clades occurring approximately 6 to 10 million years ago (Mya), coinciding with the formation of the Amazon River and several other river capture events in South America. The reconstruction of ancestral areas and karyotype, combined with the identification of shared and specific sex-linked markers, suggests that the Harttia ancestor occupied either the South and Southeast Atlantic drainages or the Eastern Amazon, with a karyotype of 2n = 58 and a homomorphic XY system. Our findings indicate the recent and independent emergence of two distinct multiple sex chromosome systems at ∼5 Mya for X ₁ X ₂ Y and ∼1 Mya for XY ₁ Y ₂ , which accelerate speciation rates in the genus. The evolution of sex chromosomes in Harttia is followed not only by structural rearrangements but also by the putative recruitment of genes associated with reproductive and physiological functions, as indicated by gene ontology analysis. Together, these findings underscore the potential contribution of multiple sex chromosome systems and their turnovers in accelerating speciation rates in teleosts.