Cytogenetic survey reveals geographic variation in B chromosomes in Paraná River fish

A cytogenetic study of 148 Prochilodus lineatus collected from seven localities in the Paraná River basin found a highly conserved standard karyotype but substantial geographic variation in the number and morphology of B chromosomes. All individuals had a diploid chromosome number of 2n = 54, a fundamental number of 108, and only metacentric and submetacentric chromosomes in the standard complement.

The researchers obtained chromosome preparations using lymphocyte cultures and examined the samples with conventional staining, C-banding, and silver staining for nucleolus organizer regions (NORs). C-banding showed heterochromatin confined to the centromeric portions of the standard chromosomes, with no differences among populations. Every individual had one NOR block on the long arm of a pair of submetacentric chromosomes, while the B chromosomes lacked NOR signals and were completely heterochromatic.

Despite the conserved basic karyotype, the sampled populations differed in their B-chromosome profiles. The Apa River population was the only one in which all analyzed individuals lacked B chromosomes. Mogi Guaçu, Sapucaí, and Grande contained the three previously described morphologies: small acrocentric, medium metacentric, and large submetacentric B chromosomes. Metacentric variants predominated in the Paraná population, which also included one individual with an acrocentric B chromosome.

Only metacentric B chromosomes were observed at the two sampling points in the Batalha River basin, Reginópolis and Bauru. A Reginópolis individual carried a previously unreported metacentric macrochromosome B, which was also completely heterochromatic. One-way analysis of variance found significant differences among localities for the frequencies of metacentric, submetacentric, and acrocentric variants. The respective statistics were F = 18.1307 for metacentric, F = 6.5932 for submetacentric, and F = 8.1826 for acrocentric B chromosomes, with P < 0.0001 and six degrees of freedom in each comparison.

Earlier studies cited by the authors provide a possible framework for these geographic differences. The metacentric B chromosome is the only variant in P. lineatus reported to have a transmission rate above Mendelian expectations, with kb = 0.587, whereas the acrocentric and submetacentric variants have lower values of 0.333 and 0.385, respectively, consistent with elimination during transmission. The new observations are compatible with accumulation of the metacentric variant and the apparent disappearance of the other two from the Paraná, Reginópolis, Bauru, and Apa populations. This is a spatial pattern in the present samples, not direct evidence of a decline through time.

All three morphologies share repetitive sequence content, and previous fluorescence in situ hybridization work has located satellite DNA sequence PliSat05-178 on the B chromosomes and in the telomeric region of autosomal pair 4. Repetitive sequences are also shared by B chromosomes in P. lineatus, P. costatus, and P. argenteus. The authors therefore interpret the common Prochilodus B chromosomes as having a single origin before the diversification of at least these three carrier species. Within P. lineatus, the proposed sequence is an ancestral acrocentric form giving rise to an isochromosome and the metacentric variant, with the submetacentric form derived subsequently.

The absence of B chromosomes in the Apa population remains open to two explanations in the authors’ assessment. Either the elements were eliminated from that historically isolated population, or they were never present there; they reject the second explanation because the shared repetitive content indicates that the B chromosomes arose long before diversification within Prochilodus. The Apa population had been isolated above Sete Quedas waterfall, which was destroyed during construction of the Itaipu hydroelectric plant. The authors also note that B chromosomes could appear there through contact with fish from other populations, although the present survey does not establish that this has occurred or identify a genetic-introduction mechanism.

Geographic variation in B-chromosome prevalence is not unique to P. lineatus. In the characid fish Psalidodon paranae, reported B-chromosome carrier frequencies in three stretches of the Cascatinha stream ranged from 65.7% near the source to 10% in each of the two downstream stretches. The authors also cite evidence from grasshoppers in which nonfunctional microspermatids arise during spermiogenesis and from P. paranae in which polar-body elimination has been associated with lower transmission from B-carrying females.

This was a geographically bounded cytogenetic survey rather than a direct test of the mechanisms driving those differences. It included 148 fish from seven sampling points, with sample sizes ranging from eight at Bauru to 32 at Mogi Guaçu. The study did not directly measure transmission rates, meiotic drive, historical change, or fitness effects in the newly sampled populations, and the proposed evolutionary sequence for the variants remains an interpretation based on chromosome structure, repetitive DNA, and earlier inheritance studies.

Subject of Research: Cytogenetic variation in B chromosomes of Prochilodus lineatus across the Paraná River basin

Article Title: Evolutionary dynamics of the B chromosomes in the fish species Prochilodus lineatus Valenciennes, 1837 of the Paraná River Basin

Article References: Penitente, M., Goes, C. A. G., dos Santos, R. Z., Utsunomia, R., Foresti, F., & Porto-Foresti, F. (2025). Evolutionary dynamics of the B chromosomes in the fish species Prochilodus lineatus Valenciennes, 1837 of the Paraná River Basin. Comparative Cytogenetics, 19, 1-12. https://doi.org/10.3897/compcytogen.19.135127

Image Credits: AI Generated

DOI: 10.3897/compcytogen.19.135127

Keywords: Prochilodus lineatus, B chromosomes, cytogenetics, Paraná River basin, fish karyotype, chromosome variants, heterochromatin, population variation, meiotic drive, Evolutionary, dynamics, chromosomes