Intrachromosomal rearrangements in two representatives of the genus Saltator (Thraupidae, Passeriformes) and the occurrence of heteromorphic Z chromosomes

Abstract

Saltator is a genus within family Thraupidae, the second largest family of Passeriformes, with more than 370 species found exclusively in the New World. Despite this, only a few species have had their karyotypes analyzed, most of them only with conventional staining. The diploid number is close to 80, and chromosome morphology is similar to the usual avian karyotype. Recent studies using cross-species chromosome painting have shown that, although the chromosomal morphology and number are similar to many species of birds, Passeriformes exhibit a complex pattern of paracentric and pericentric inversions in the chromosome homologous to GGA1q in two different suborders, Oscines and Suboscines. Hence, considering the importance and species richness of Thraupidae, this study aims to analyze two species of genus Saltator, the golden-billed saltator (S. aurantiirostris) and the green-winged saltator (S. similis) by means of classical cytogenetics and cross-species chromosome painting using Gallus gallus and Leucopternis albicollis probes, and also 5S and 18S rDNA and telomeric sequences. The results show that the karyotypes of these species are similar to other species of Passeriformes. Interestingly, the Z chromosome appears heteromorphic in S. similis, varying in morphology from acrocentric to metacentric. 5S and 18S probes hybridize to one pair of microchromosomes each, and telomeric sequences produce signals only in the terminal regions of chromosomes. FISH results are very similar to the Passeriformes already analyzed by means of molecular cytogenetics (Turdus species and Elaenia spectabilis). However, the paracentric and pericentric inversions observed in Saltator are different from those detected in these species, an observation that helps to explain the probable sequence of rearrangements. As these rearrangements are found in both suborders of Passeriformes (Oscines and Suboscines), we propose that the fission of GGA1 and inversions in GGA1q have occurred very early after the radiation of this order.

Chromosome Painting in Tyrant Flycatchers Confirms a Set of Inversions Shared by Oscines and Suboscines (Aves, Passeriformes)

“…Besides the confirmation of breakpoints of ancient syntenic groups, one of the most interesting findings is the detection of both paracentric and pericentric inversions in the ancestral pair 1 (GGA1q), observed both in Oscines and Suboscines [Kretschmer et al, 2014dos Santos et al, 2015dos Santos et al, , 2017. As the results in Suboscines were based on only 1 species, E. spectabilis , our data confirm that these inversions are present in different subfamilies among Tyrannidae and must have occurred before the separation of Suboscines and Oscines, 20 million years ago [Ohlson et al, 2013].…”

“…S. icterophrys and P. sulphuratus show only 1 pair of microchromosomes with 18S rDNA. This is the most common situation observed among birds, including basal groups such as G. gallus [Ladjali-Mohammedi et al, 1999], and also in other Passeriformes [Kretschmer et al, 2014;dos Santos et al, 2015] and New World vultures [Tagliarini et al, 2009]. This condition -1 cluster of 18S rDNA located in a pair of microchromosomes -seems to be a plesiomorphic state, while a higher number of clusters represent a derived state, as in the case of S. subcristata , in which we found 2 pairs of microchromosomes with clusters of 18S rRNA genes.…”

“…sulphuratus and S. subcristata have macrochromosomes with the same morphology, despite different diploid numbers. The analyses of classical cytogenetic data and FISH experiments show that these species retain a chromosome formula which is similar not only to other Tyrannidae, but also to other Oscines, with the first pair being submetacentric (corresponding to GGA2) and the presence of a centric fission in the ancestral pair 1, followed by a number of paracentric inversions, especially in the segment corresponding to GGA1q [Gunski et al, 2000;Kretschmer et al, 2014Kretschmer et al, , 2015dos Santos et al, 2015dos Santos et al, , 2017. Thus, the difference of diploid numbers must be due to rearrangements involving microchromosomes.…”

“…The results showed a chromosomal organization similar to other Passeriformes belonging to the suborder Oscines, suggesting that the fissions and paracentric inversions detected by FISH had occurred before the divergence of Passeriformes into 2 groups . Hence, the fission of the ancestral syntenic group corresponding to chicken ( Gallus gallus ) chromosome 1 (GGA1), and the occurrence of numerous inversions, both paracentric and pericentric in GGA1q, may be a cytogenetic signature for Passeriformes [Kretschmer et al, 2014dos Santos et al, 2015dos Santos et al, , 2017. The analysis of other species of tyrants is necessary to corroborate this notion and define the chromosomal evolutionary history of Passeriformes.…”

Heterologous Synapsis and Crossover Suppression in Heterozygotes for a Pericentric Inversion in the Zebra Finch

“…Here, we show that early non-homologous synapsis and crossover disruption seems to be prevalent in heterozygotes for intrachromosomal rearrangements among birds, with the possible result of reduced deleterious effects and minimal reproductive impairment in carriers. These observations are significant because comparative genomic and cytogenetic studies show that inversions are especially common during the evolution of avian karyotypes in distantly related taxa [Skinner and Griffin, 2012;Kawakami et al, 2014], as well as in closely related species [Kretschmer et al, 2014;Dos Santos et al, 2015]. Moreover, it has been suggested that the relatively high rate of inversions detected in interspecific comparisons agrees with the observation of segregating inversion polymorphisms among birds [Ellegren, 2013].…”