Chromosomal rearrangements and the first indication of an ♀X₁X₁X₂X₂/♂X₁X₂Y sex chromosome system in Rineloricaria fishes (Teleostei: Siluriformes)

Abstract

Rineloricaria is the most diverse genus within the freshwater fish subfamily Loricariinae, and it is widely distributed in the Neotropical region. Despite limited cytogenetic data, records from southern and south‐eastern Brazil suggest a high rate of chromosomal rearrangements in this genus, mirrored in remarkable inter‐ and intraspecific karyotype variability. In the present work, we investigated the karyotype features of Rineloricaria teffeana, an endemic representative from northern Brazil, using both conventional and molecular cytogenetic techniques. We revealed different diploid chromosome numbers (2n) between sexes (33♂/34♀), which suggests the presence of an ♀X1X1X2X2/♂X1X2Y multiple sex chromosome system. The male‐limited Y chromosome was the largest and the only biarmed element in the karyotype, implying Y‐autosome fusion as the most probable mechanism behind its origination. C‐banding revealed low amounts of constitutive heterochromatin, mostly confined to the (peri)centromeric regions of most chromosomes (including the X2 and the Y) but also occupying the distal regions of a few chromosomal pairs. The chromosomal localization of the 18S ribosomal DNA (rDNA) clusters revealed a single site on chromosome pair 4, which was adjacent to the 5S rDNA cluster. Additional 5S rDNA loci were present on the autosome pair 8, X1 chromosome, and in the presumed fusion point on the Y chromosome. The probe for telomeric repeat motif (TTAGGG)n revealed signals of variable intensities at the ends of all chromosomes except for the Y chromosome, where no detectable signals were evidenced. Male‐to‐female comparative genomic hybridization revealed no sex‐specific or sex‐biased repetitive DNA accumulations, suggesting a presumably low level of neo‐Y chromosome differentiation. We provide evidence that rDNA sites might have played a role in the formation of this putative multiple sex chromosome system and that chromosome fusions originate through different mechanisms among different Rineloricaria species.

Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged AfricanNothobranchiuskillifish karyotypes

“…In favor of the second possibility, telomeric FISH did not yield signals even on natural chromosomal ends of large metacentric pair in N. cardinalis, regardless the exposition time. Similar situation has been recently recorded also in Neotropical siluriform fish Rineloricaria teffeana [Marajó et al, 2023].…”

“…The absence of detectable telomeric repeats in expected/supposed fusion points across all herein studied Nothobranchius species suggests that unlike some other fish groups (e.g., [Sember et al, 2015; Marajó et al, 2023]) chromosome rearrangements in Nothobranchius seem to follow generally similar mechanistic trajectories and may be driven by similar causes. Fusions of chromosomes with broken or too short telomeres may result from various aberrant events such as replication fork stalling/collapse or telomere uncapping (i.e.…”

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

“…In favor of the second possibility, telomeric FISH did not yield signals even on natural chromosomal ends of large metacentric pair in N. cardinalis , regardless of the exposition time. A similar situation has also been recently recorded in the Neotropical siluriform fish Rineloricaria teffeana (Marajó et al, 2023).…”

“…The absence of detectable telomeric repeats in expected/supposed fusion points across all herein studied Nothobranchius species suggests that unlike some other fish groups (e.g., Marajó et al, 2023; Sember et al, 2015), chromosome rearrangements in Nothobranchius seem to follow generally similar mechanistic trajectories and may be driven by similar causes. Fusions of chromosomes with broken or too short telomeres may result from various aberrant events such as replication fork stalling/collapse or telomere uncapping (i.e., loss of associated protective proteins) (Lazzerini‐Denchi & Sfeir, 2016; Stroik & Hendrickson, 2020).…”

“…The absence of detectable telomeric repeats may therefore mean their (i) complete loss prior/during the rearrangement, (ii) too low copy number to be detected by FISH, and/or (iii) gradual sequence erosion by mutations during evolution (Ocalewicz, 2013;Slijepcevic, 1998). In favor of the second possibility, The absence of detectable telomeric repeats in expected/supposed fusion points across all herein studied Nothobranchius species suggests that unlike some other fish groups (e.g., Maraj o et al, 2023;Sember et al, 2015), chromosome rearrangements in Nothobranchius seem to follow generally similar mechanistic trajectories and may be driven by similar causes. Fusions of chromosomes with broken or too short telomeres may result from various aberrant events such as replication fork stalling/collapse or telomere uncapping (i.e., loss of associated protective proteins) (Lazzerini-Denchi & Sfeir, 2016;Stroik & Hendrickson, 2020).…”