Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci

• Published in: Chromosome research Vol. 30; no. 4; pp. 309 - 333
• Main Authors: Štundlová, Jana, Hospodářská, Monika, Lukšíková, Karolína, Voleníková, Anna, Pavlica, Tomáš, Altmanová, Marie, Richter, Annekatrin, Reichard, Martin, Dalíková, Martina, Pelikánová, Šárka, Marta, Anatolie, Simanovsky, Sergey A., Hiřman, Matyáš, Jankásek, Marek, Dvořák, Tomáš, Bohlen, Joerg, Ráb, Petr, Englert, Christoph, Nguyen, Petr, Sember, Alexandr
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 01-12-2022; Springer Nature B.V
• Subjects: African People; Animal Genetics and Genomics; Animals; Artificial chromosomes; Bacterial artificial chromosomes; Biomedical and Life Sciences; Cell Biology; Comparative Genomic Hybridization; Cyprinodontidae; Cytogenetics; Divergence; Evolution, Molecular; Fluorescence in situ hybridization; Fundulidae - genetics; Human Genetics; Humans; In Situ Hybridization, Fluorescence; Inversion; Killifishes - genetics; Life Sciences; Meiosis; Meiotic drive; MLH1 protein; Nothobranchius furzeri; Plant Genetics and Genomics; Recombination; rRNA; Satellite DNA; Satellite RNA; Sequence analysis; Sex chromosomes; Sex Chromosomes - genetics; Sibling species; Single-nucleotide polymorphism; Y Chromosome - genetics; Y chromosomes; Sex chromosome degeneration; Sex chromosome polymorphism; Inversion; RepeatExplorer; Recombination suppression; Repeatome
• ISSN: 0967-3849; 1573-6849
• DOI: 10.1007/s10577-022-09707-3

Homomorphic sex chromosomes and their turnover are common in teleosts. We investigated the evolution of nascent sex chromosomes in several populations of two sister species of African annual killifishes,
Nothobranchius furzeri
and
N. kadleci
, focusing on their under-studied repetitive landscape. We combined bioinformatic analyses of the repeatome with molecular cytogenetic techniques, including comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, ribosomal RNA genes (rDNA) and bacterial artificial chromosomes (BACs), and immunostaining of SYCP3 and MLH1 proteins to mark lateral elements of synaptonemal complexes and recombination sites, respectively. Both species share the same heteromorphic XY sex chromosome system, which thus evolved prior to their divergence. This was corroborated by sequence analysis of a putative master sex determining (MSD) gene
gdf6Y
in both species. Based on their divergence, differentiation of the XY sex chromosome pair started approximately 2 million years ago. In all populations, the
gdf6Y
gene mapped within a region rich in satellite DNA on the Y chromosome long arms. Despite their heteromorphism, X and Y chromosomes mostly pair regularly in meiosis, implying synaptic adjustment. In
N. kadleci
, Y-linked paracentric inversions like those previously reported in
N. furzeri
were detected. An inversion involving the MSD gene may suppress occasional recombination in the region, which we otherwise evidenced in the
N. furzeri
population MZCS-121 of the Limpopo clade lacking this inversion. Y chromosome centromeric repeats were reduced compared with the X chromosome and autosomes, which points to a role of relaxed meiotic drive in shaping the Y chromosome repeat landscape. We speculate that the recombination rate between sex chromosomes was reduced due to heterochiasmy. The observed differences between the repeat accumulations on the X and Y chromosomes probably result from high repeat turnover and may not relate closely to the divergence inferred from earlier SNP analyses.