Sex chromosome turnover linked to faster speciation in armored catfish

A genus of Neotropical armored catfish may owe its remarkable diversity, at least in part, to an unusual habit: repeatedly rebuilding its sex chromosomes. A new genome-wide study of the catfish genus Harttia, published in Biology Direct, reports that lineages carrying multiple sex chromosome systems show markedly higher inferred speciation rates than relatives with simple sex chromosomes, and that these complex systems arose independently at least twice within the past few million years. The work provides the first genome-wide evolutionary framework for a group that has long puzzled cytogeneticists.

Harttia, a monophyletic genus of 28 valid species distributed across rheophilic habitats of the Brazilian and Guiana Shields, holds the record among fishes for diversity of multiple sex chromosome systems. Roughly 28 percent of its species display heteromorphic sex chromosomes, a proportion matched among fishes only by Nothobranchius killifishes. Previous conventional and molecular cytogenetic work had already revealed an exceptional range of diploid numbers, from 52 to 62 chromosomes, and two independent male-heterogametic systems: the XX/XY1Y2 system in species from South and Southeast Brazil, and the X1X1X2X2/X1X2Y system in Amazonian species. What remained unresolved was how these systems originated and whether their repeated turnover contributed to the diversification of the genus.

To address these questions, researchers generated DArTseq data, a genome-wide complexity-reduction sequencing approach well suited to non-model organisms lacking reference genomes, for 107 individuals from 17 Harttia species plus one outgroup species, Farlowella sp. The sequencing produced 95,305 SNPs and 282,275 SilicoDArT presence-absence loci. After stringent filtering, a phylogeny built from 24,858 SNP markers, roughly 1,381 SNPs per species, resolved three major Harttia clades, each with strong geographic coherence: Clade I from Guiana Shield drainages, Clade II from Amazonian Brazilian Shield drainages including the Xingu, Tapajós and Tocantins-Araguaia basins, and Clade III from Southeastern and South Atlantic drainages and the La Plata basin.

The time-calibrated tree tells a story of recent, geologically synchronized radiation. Harttia and Farlowella diverged approximately 29.5 million years ago, but the three Harttia clades split within the last 10 million years: Clade I separated about 10 million years ago, and Clades II and III diverged roughly 7.9 million years ago. The authors link this timing to major Neotropical drainage rearrangements, including the Miocene uplift of the Andes, the redirection of proto-Tapajós, proto-Xingu and proto-Tocantins-Araguaia river courses in the late Miocene, and the uplift of the Serra do Mar and Serra da Mantiqueira ranges, which isolated portions of the La Plata Basin from Atlantic drainages. Biogeographical modeling with the DIVALIKE model, selected as the best fit by AICc scores, placed the most recent common ancestor of the genus in the Southern or Southeastern Atlantic drainages, with Clade II later confined to the Amazon Brazilian Shield.

The chromosome-number story proved equally dynamic. Ancestral reconstruction under the best-fitting Dys model in ChromEvol supported an ancestral diploid number of 2n = 58 for Harttia, corroborating earlier hypotheses based on comparative cytogenetics. Subsequent karyotype reductions, mostly via centric fusions, produced 2n = 56 in species such as H. loricariformis, H. villasboas and H. duriventris, and 2n = 54 in H. rondoni and Harttia sp. 3. Notably, these rearrangements did not involve the chromosomal components underlying the multiple sex chromosome systems, indicating that autosomal and sex chromosome evolution proceeded largely independently in this genus.

Sex-linked markers provided the molecular key to the origins of the multiple systems. Applying a Bonferroni-corrected threshold across the full 95,305-SNP dataset, the team identified 443 candidate sex-linked markers: 95 XY and 16 ZW markers from the SNP dataset, and 316 XY and 16 ZW markers from the SilicoDArT dataset. Shared sex-linked markers, defined at a 100 percent similarity threshold, occurred only within two groups, one comprising H. carvalhoi and H. intermontana with the XY1Y2 system, and another comprising a subset of Clade II species with the X1X2Y system, and never between the groups. This pattern points to independent origins for the two multiple sex chromosome systems. Integration with previous cytogenetic evidence is consistent with an ancestral homomorphic XY system that subsequently underwent independent chromosome rearrangements, a Y-autosome translocation in the southern lineage and fission or sex-determining gene turnover in the Amazonian lineage, generating the different multiple systems in distinct lineages.

The most striking result came from state-dependent diversification modeling. Using the Binary State Speciation and Extinction model, the authors estimated that lineages with simple sex chromosomes speciate at a rate of 0.032 per lineage per unit time, with a 95 percent confidence interval of 0.026 to 0.290, whereas lineages with multiple sex chromosomes show a speciation rate of 0.941, with a confidence interval of 0.485 to 3.064. A likelihood ratio test comparing models with equal and unequal speciation rates yielded a p-value of 0.005, suggesting a statistically significant association between the presence of multiple sex chromosomes and elevated diversification. Lineage-through-time analysis reinforced the pattern, revealing two significant shifts in the number of lineages, at roughly 2.5 and 1.3 million years ago, coinciding with the splits of clades carrying multiple sex chromosome systems.

The authors propose a plausible mechanistic link. Multiple sex chromosome systems arising through rearrangements can generate postzygotic isolation through segregation incompatibilities, suppress recombination near rearranged regions and thereby reduce gene flow, and allow genes contributing to reproductive isolation to accumulate on neo-sex chromosomes. Similar processes have been documented in sticklebacks and proposed for Brenthis butterflies, African cichlids and rock wallabies. In Harttia, these turnover events occurred within an exceptionally short window of roughly 4 million years, a tempo the authors describe as unmatched among reported cases of recurrent sex chromosome turnover in plants, fish and reptiles.

The study is careful to state its limitations. Candidate sex-linked markers were identified from only three individuals per sex per species, and the authors explicitly note that larger sampling is needed for better statistical confidence. Because Harttia lacks assembled genomes, the markers were cross-mapped to the two available chromosome-level loricariid genomes, Pterygoplichthys pardalis and P. disjunctivus, which diverged from Harttia tens of millions of years ago and lack identified sex chromosomes. Markers mapped to multiple chromosomes in both species, with no clear one-to-one conservation of a single sex-linked region, a result the authors interpret as more consistent with genome-wide conservation of short marker sequences than with conservation of an ancestral sex chromosome. They stress that definitive reconstruction of sex chromosome evolution will require chromosome-level genomes and larger population samples for the relevant Harttia lineages.

The conclusions are correspondingly measured. The authors write 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 the association, and noting that the causal relationship remains unresolved. The phylogeny also yielded an unexpected taxonomic finding: Harttia sp. 2, recovered as deeply divergent with an estimated split around 25 million years ago and lacking sex-linked markers, shares a karyotype with H. absaberi, a species previously suggested to belong outside Harttia, supporting the hypothesis that both may not belong to Harttia sensu stricto. For evolutionary biologists, the message is that Harttia now stands as a powerful model for investigating how sex chromosome turnover, chromosome evolution and landscape history jointly shape biodiversity, with the caveat that association, however statistically strong, is not yet demonstrated causation.

Subject of Research: Genome-wide analysis of sex chromosome turnover and diversification in the Neotropical armored catfish genus Harttia

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

Article References: Sassi, F. D. M. C., de Souza, F. H. S., Perez, M. F., Shams, F., Ezaz, T., Deon, G. A., Liehr, T., Xu, L., & Cioffi, M. D. B. (2026). Rapid turnover of sex chromosomes is associated with speciation in Neotropical armored catfish Harttia (Siluriformes, Loricariidae). Biology Direct, 21(1), Article 211. https://doi.org/10.1186/s13062-026-00994-y

Image Credits: AI Generated

DOI: 10.1186/s13062-026-00994-y

Keywords: Harttia, armored catfish, sex chromosomes, speciation, DArTseq, Neotropical fishes, phylogenetics, BiSSE, karyotype evolution, biogeography, Loricariidae, sex-linked markers