Biology subjects

Rab, P.

Publications and source records attributed to Rab, P..

3 recordsLinked to original sources

bioRxiv2024

Sex chromosome turnover in African annual killifishes of the genus Nothobranchius

Sex chromosomes of teleost fishes often have low levels of differentiation and undergo frequent turnovers. Annual Nothobranchius killifishes comprise representatives with male-heterogametic XY or X1X2Y sex chromosome systems, scattered across their phylogeny, nested within species lacking cytologically detectable sex chromosomes. They thus provide a suitable system to study sex chromosome evolution and turnover. Here, we combined molecular cytogenetics and genomic analyses to examine several multiple sex chromosome systems in Nothobranchius spp. and their outgroup Fundulosoma thierryi. We used fluorescence in situ hybridization with three sex chromosome-specific painting probes and bacterial artificial chromosomes (BAC) bearing eight orthologues of genes found to be repeatedly co-opted as master sex determining (MSD) genes in fishes. Our results suggest at least four independent origins of sex chromosomes in the genus Nothobranchius. The synteny block carrying amhr2 gene was shared by X1X2Y systems of N. brieni, N. guentheri and N. lourensi, but the autosomal additions and the overall neo-Y chromosome structure differed among these species. On the other hand, gdf6 gene was localized to neo-Y of F. thierryi. None of the mapped MSD gene candidates seems to determine sex in N. ditte. We further sequenced genomes of F. thierryi female and N. guentheri male by long-read platforms and performed analyses of male and female Pool-seq data and coverage to delimit their non-recombining regions, determine degree of their differentiation, and thus complement the cytogenetic data in assessing potential MSD genes. We found low level of sex chromosomes differentiation in F. thierryi. In N. guentheri, however, we identified two distinct evolutionary strata on neo-Y. The amhr2 gene resides in the younger stratum and has low allelic variation, which questions its role in sex determination.

evolutionary biology↗

bioRxiv2023

Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged African Nothobranchius killifish karyotypes

Repetitive DNA may have significant impact on genome evolution. African annual killifishes of the genus Nothobranchius (Teleostei: Nothobranchiidae), which has adapted to temporary water pools in African savannahs, possess genomes with high repeat content. They are also characterized by rapid karyotype and sex chromosome evolution but the role of genome repeats in these processes remains largely unknown. Here, we analyzed the distribution of telomeric (TTAGGG)n repeat and Nfu-SatC satellite DNA (isolated formerly from N. furzeri) by fluorescence in situ hybridization in representatives across the Nothobranchius phylogeny (15 species), and with Fundulosoma thierryi as an outgroup. All analyzed taxa shared the presence of Nfu-SatC repeat but with diverse organization and distribution on chromosomes (from small clusters scattered genome-wide, to large localized accumulations, or a combined pattern). Nfu-SatC landscape was similar in conspecific populations of N. guentheri and N. melanospilus but slightly-to-moderately differed between populations of N. pienaari, and between closely related N. kuhntae and N. orthonotus. Inter-individual variability in Nfu-SatC patterns was found in N. orthonotus and N. krysanovi, including distinct segments present often in heterozygous condition. We revealed mostly no sex-linked patterns of studied repeats distribution in any of the sampled species including those with known sex chromosomes. Only in N. brieni (having an X1X2Y multiple sex chromosome system), Nfu-SatC probe covered substantial portion of the Y chromosome, similarly as formerly found in N. furzeri and N. kadleci (XY sex chromosomes), sister species not closely related to N. brieni. All studied species further shared patterns of telomeric FISH, with expected signals at the ends of all chromosomes and no additional interstitial telomeric sites. In summary, we revealed i) the presence of conserved satDNA class in Nothobranchius clade (a rare pattern among ray-finned fishes), ii) independent trajectories of Nothobranchius sex chromosome diferentiation, with recurrent and convergent accumulation of Nfu-SatC on the Y chromosome in some species, and iii) genus-wide shared propensity to loss of telomeric repeats during the mechanism of interchromosomal rearrangements. Collectively, our findings advance our understanding of genome structure, mechanisms of karyotype reshuffling and sex chromosome differentiation in Nothobranchius killifishes from the genus-wide perspective.

genetics↗

bioRxiv2022

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

Repetitive DNA represents an important driver of sex chromosome differentiation. Yet, repetitive sequences tend to be misrepresented or overlooked in genomic studies. We analysed repetitive DNA landscape of sex chromosomes in several populations of a turquoise killifish Nothobranchius furzeri and its sister species N. kadleci (Teleostei: Nothobranchiidae), representatives of African annual killifishes with high rate of karyotype and sex chromosome evolution. We combined bioinformatic analyses of repeatome with molecular cytogenetic techniques such as comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, genes for ribosomal RNAs (rDNA) and bacterial artificial chromosomes (BACs) and immunostaining of SYCP3 and MLH1 proteins, which marked lateral elements of synaptonemal complexes and recombination sites, respectively. We revealed that N. furzeri and N. kadleci share the XY sex chromosome system, which is thus much older than previously assumed. Sex chromosomes are mostly heteromorphic as evidenced by distinct distribution of satellite DNAs and major rDNA. Yet, the heteromorphic XY sex chromosomes pair almost exclusively regularly in meiosis, which implies synaptic adjustment. Physical mapping of BACs identified inversions on Y chromosomes of the N. kadleci populations, akin to the pattern previously reported in N. furzeri. Yet, repetitive DNA landscape of X and Y sex chromosomes either diverged in parallel in populations of both species or it evolved in their common ancestor and thus predates the inversions. The observed differentiation via repeat repatterning thus cannot be explained by the classical sexually antagonistic model. Rather, we hypothesized that relaxed meiotic drive and recombination reduced by neutral processes could drive changes in repeatome and secondary inversions could be maintained by sexually antagonistic regulatory effects resulting from early evolution of dosage compensation. Author summaryEarly differentiation of sex chromosomes is not yet satisfactorily understood despite intensive research effort. Homomorphic sex chromosomes and their rapid turnover are common in teleost fishes, which makes them excellent models for studying evolution of nascent sex chromosomes. We investigated sex chromosomes in several populations of two sister species of African annual killifishes, Nothobranchius furzeri and N. kadleci, particularly their repetitive landscape, which was misrepresented in previous genomic studies. Combination of cytogenetic and genomic approaches revealed that both species share heteromorphic XY sex chromosome system. The N. furzeri XY sex chromosomes thus evolved earlier than previously expected. In N. kadleci, Y-linked inversions analogous to those reported in N. furzeri were detected. Changes in repetitive DNA distribution on sex chromosomes are either convergent or occurred in a common ancestor of both species, prior to the inversion events. The observed sex chromosome differentiation on repetitive DNA level thus cannot be reconciled with the classical theoretical model of sex chromosome evolution driven by sexually antagonistic selection. We invoke alternative explanations such as relaxed meiotic drive and recombination reduced by neutral processes, and we hypothesize that secondary inversions could be maintained by early evolution of dosage compensation resulting in sexually antagonistic regulatory effects.

evolutionary biology↗