Chromosomal Evolution and Evolutionary Relationships of Lebiasina Species (Characiformes, Lebiasinidae)

Abstract

We present the first cytogenetic data for Lebiasina bimaculata and L. melanoguttata with the aim of (1) investigating evolutionary events within Lebiasina and their relationships with other Lebiasinidae genera and (2) checking the evolutionary relationships between Lebiasinidae and Ctenoluciidae. Both species have a diploid number 2n = 36 with similar karyotypes and microsatellite distribution patterns but present contrasting C-positive heterochromatin and CMA3+ banding patterns. The remarkable interstitial series of C-positive heterochromatin occurring in L. melanoguttata is absent in L. bimaculata. Accordingly, L. bimaculata shows the ribosomal DNA sites as the only GC-rich (CMA3+) regions, while L. melanoguttata shows evidence of a clear intercalated CMA3+ banding pattern. In addition, the multiple 5S and 18S rDNA sites in L. melanogutatta contrast with single sites present in L. bimaculata. Comparative genomic hybridization (CGH) experiments also revealed a high level of genomic differentiation between both species. A polymorphic state of a conspicuous C-positive, CMA3+, and (CGG)n band was found only to occur in L. bimaculata females, and its possible relationship with a nascent sex chromosome system is discussed. Whole chromosome painting (WCP) and CGH experiments indicate that the Lebiasina species examined and Boulengerella maculata share similar chromosomal sequences, thus supporting the relatedness between them and the evolutionary relationships between the Lebiasinidae and Ctenoluciidae families.

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

“…Altogether with Ctenoluciidae [37], this pattern can be considered as symplesiomorphy for both families. Although 5S rDNA displays a more dynamic evolution, with both terminal and interstitial signals among lebiasinids ( [19][20][21][22], this study), it is noteworthy that N. unifasciatus underwent structural chromosome rearrangements involving both 18S and 5S rDNA loci, which have led to a derived pattern of rDNA distribution in this species. It is a rather expected scenario for N. unifasciatus, since this species exhibits the lowest 2n among Lebiasinidae fishes (2n = 22) and hence it may be speculated that the proximal 18S and 5S rDNA sites found in N. unifasciatus might rather represent hallmarks of fusion, suggesting the probable direction of chromosome change in this genus.…”

“…More specifically, high rate of repetitive DNA dynamics and the occasional emergence of neo-sex chromosomes were found among four Pyrrhulina taxa; one of them may represent a new, yet undescribed species [19,20]. Furthermore, contrasting patterns of repetitive DNA content and distribution as well as a putative nascent sex chromosome system were also reported for Lebiasina species, supporting at the same time relationships between the Lebiasinidae and Ctenoluciidae families [21]. In addition, the first molecular cytogenetic report on Copeina species is filling another gap in this research [22].…”

“…In the case of rDNAs, this may be possibly linked with the susceptibility of these tandemly repeated clusters to double-stranded DNA breaks, perhaps resulting from (1) a frequent rRNA transcription and thus break-prone R-loop emergence, (2) intermingling of NOR (Nuclear Organizer Region)-bearing chromosomes in the interphase nucleus, or (3) possible association of rDNA-bearing sites during the meiotic prophase I [42][43][44][45][46][47][48]. With a few exceptions, the terminal position of the 18S rDNA loci on chromosomes appears to be a common feature for all Lebiasinidae genera analyzed up to now (i.e., Nannostomus, Pyrrhulina, Lebiasina, and Copeina) ( [19][20][21][22], this study). Altogether with Ctenoluciidae [37], this pattern can be considered as symplesiomorphy for both families.…”

“…For this, the modal 2n of characiform fishes and the phylogenetic relationship of Nannostomus with the nearest lebiasinid lineages may provide a first useful indication (the principle reviewed in Dobigny et al [35]). Thus, taking into account that (1) the modal 2n for characiforms very likely may be 2n = 54 [36], (2) Lebiasina, the most basal genus of Lebiasinidae [14] is characterized by 2n = 36 [21], and (3) the same 2n is also present among Ctenoluciidae species [37], a probable sister family of Lebiasinidae [38], we can infer that the reduction of 2n among the Nannostomus species was most likely achieved by a series of chromosome fusions. Specifically, according to Benzaquem et al [15], N. unifasciatus, with 2n = 22 and with a karyotype formed exclusively by bi-armed chromosomes, is phylogenetically closely related to N. beckfordi, which possesses 2n = 44 and a karyotype formed by acrocentric chromosomes only.…”

“…In contrast to relative stability of the 2n in Copeina, Lebiasina and Pyrrhulina species karyotyped to date [16][17][18][19][20][21][22], representatives of Copella and Nannostomus display remarkable karyotype variability [16,18]. Indeed, even from limited karyotype data, it can be inferred that Nannostomus exhibits a wide range of 2n, from 22 (in N. unifasciatus) to 46 (in N. trifasciatus) [16,18,23], suggesting an important role of Robertsonian rearrangements in its karyotype differentiation.…”