Turnover of multiple sex chromosomes in Harttia catfish (Siluriformes, Loricariidae): a glimpse from whole chromosome painting

Francisco de Menezes Cavalcante Sassi; Geize Aparecida Deon; Alexandr Sember; Thomas Liehr; Osvaldo Takeshi Oyakawa; Orlando Moreira Filho; Luiz Antonio Carlos Bertollo; Marcelo Ricardo Vicari; Marcelo de Bello Cioffi

doi:10.3389/fgene.2023.1226222

Turnover of multiple sex chromosomes in Harttia catfish (Siluriformes, Loricariidae): a glimpse from whole chromosome painting

Front Genet. 2023 Jul 28:14:1226222. doi: 10.3389/fgene.2023.1226222. eCollection 2023.

Authors

Francisco de Menezes Cavalcante Sassi¹, Geize Aparecida Deon¹, Alexandr Sember², Thomas Liehr³, Osvaldo Takeshi Oyakawa⁴, Orlando Moreira Filho¹, Luiz Antonio Carlos Bertollo¹, Marcelo Ricardo Vicari⁵, Marcelo de Bello Cioffi¹

Affiliations

¹ Laboratório de Citogenética de Peixes, Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos, Brazil.
² Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Liběchov, Czechia.
³ Institut für Humangenetik, Universitätsklinikum Jena, Jena, Germany.
⁴ Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.
⁵ Departamento de Biologia Estrutural, Molecular e Genética, Universidade Estadual de Ponta Grossa, Ponta Grossa, Brazil.

Abstract

The remarkable fish biodiversity encompasses also great sex chromosome variability. Harttia catfish belong to Neotropical models for karyotype and sex chromosome research. Some species possess one of the three male-heterogametic sex chromosome systems, XY, X₁X₂Y or XY₁Y₂, while other members of the genus have yet uncharacterized modes of sex determination. Particularly the XY₁Y₂ multiple sex chromosome system shows a relatively low incidence among vertebrates, and it has not been yet thoroughly investigated. Previous research suggested two independent X-autosome fusions in Harttia which led to the emergence of XY₁Y₂ sex chromosome system in three of its species. In this study, we investigated evolutionary trajectories of synteny blocks involved in this XY₁Y₂ system by probing six Harttia species with whole chromosome painting (WCP) probes derived from the X (HCA-X) and the chromosome 9 (HCA-9) of H. carvalhoi. We found that both painting probes hybridize to two distinct chromosome pairs in Amazonian species, whereas the HCA-9 probe paints three chromosome pairs in H. guianensis, endemic to Guyanese drainages. These findings demonstrate distinct evolutionary fates of mapped synteny blocks and thereby elevated karyotype dynamics in Harttia among the three evolutionary clades.

Keywords: WCP; chromosomal rearrangements; evolution; karyotype; microdissection.

Grants and funding

This work was supported by São Paulo Research Foundation (FAPESP) grants 2020/02681-9 and 2022/04261-2 (FS), 2020/11772-8 (MC) and Brazilian National Council for Scientific and Technological Development (CNPq), grant number 302928/2021-9 (MC). AS was supported by Czech Academy of Sciences (RVO: 67985904 of IAPG CAS, Liběchov). We also acknowledge support for TL by the German Research Foundation Projekt-Nr. 512648189 and the Open Access Publication Fund of the Thueringer Universitaets-und Landesbibliothek Jena. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), Finance Code 001. This study was supported by INCT - Peixes, funded by MCTIC/CNPq (proc. 405706/2022-7).