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Fluorescent in situ hybridization using whole-chromosome probes of Leucopternis albicollis macrochromosomes in metaphases of P. frontalis. LAL: Leucopternis albicollis.
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: Most Neotropical Psittacidae have a diploid number of 2n = 70, and a dichotomy in chromosome patterns. Long-tailed species have biarmed macrochromosomes, while short-tailed species have telo/acrocentric macrochromosomes. However, the use of chromosome painting has demonstrated that karyotype evolution in Psittacidae includes a high number of inte...
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... Genomic chromosomal rearrangement is probably an important source of the gene loss events. Massive chromosomal alterations have profoundly affected vertebrate evolution in general [27], as well as in certain lineages [28] including parrots in particular [29][30][31]. Recent advances in genomic research have allowed thorough mapping of evolutionary gene loss events affecting immune signalling [24,[32][33][34][35]. ...
... Thus, diversity in avian immune responses to peripheral stimulation remains largely unknown. Of particular relevance is the immune response regulation in species with highly rearranged genomes, such as the parrots [29,31]. ...
... Our genome-database search indicated a complete absence of functional CNR2 genes in all parrot species investigated, which contrasts with its conserved presence in all lineages closely related to parrots (i.e. the falcons, seriemas and passerines, including the zebra finch). We were able to identify putative remnants of the CNR2 pseudogene in the budgerigar genome, indicating apparent CNR2 pseudogenization following massive karyotype rearrangements early in parrot phylogeny [29,31]. Interestingly, a comparison of the karyotype localization of passerine CNR2-neighbouring genes in the budgerigar and kakapo genomes suggested two presumably independent karyotype rearrangement events in parrots resulting in the CNR2 loss. ...
In vertebrates, cannabinoids modulate neuroimmune interactions through two cannabinoid receptors (CNRs) conservatively expressed in the brain (CNR1, syn. CB1) and in the periphery (CNR2, syn. CB2). Our comparative genomic analysis indicates several evolutionary losses in the CNR2 gene that is involved in immune regulation. Notably, we show that the CNR2 gene pseudogenized in all parrots (Psittaciformes). This CNR2 gene loss occurred because of chromosomal rearrangements. Our positive selection analysis suggests the absence of any specific molecular adaptations in parrot CNR1 that would compensate for the CNR2 loss in the modulation of the neuroimmune interactions. Using transcriptomic data from the brains of birds with experimentally induced sterile inflammation we highlight possible functional effects of such a CNR2 gene loss. We compare the expression patterns of CNR and neuroinflammatory markers in CNR2-deficient parrots (represented by the budgerigar, Melopsittacus undulatus and five other parrot species) with CNR2-intact passerines (represented by the zebra finch, Taeniopygia guttata). Unlike in passerines, stimulation with lipopolysaccharide resulted in neuroinflammation in the parrots linked with a significant upregulation of expression in proinflammatory cytokines (including interleukin 1 beta (IL1B) and 6 (IL6)) in the brain. Our results indicate the functional importance of the CNR2 gene loss for increased sensitivity to brain inflammation.
... As a result of the above ancestral karyotype reconstruction , a similar pattern of chromosome organization in the presumable NGA and Neoaves ancestor (NAA) was observed. Overall, according to this gross estimate and using datasets for the 12 species produced in this and few other published studies, NGA and NAA are likely to have 29 chromosomes (autosomes), including 10 macrochromosomes (i.e., autosomes 1-9 + 4A) and 19 microchromosomes (i.e., autosomes [10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28]. Compared to the chicken karyotype, the only difference between these two karyotypes and the chicken one was that chromosome GGA4 was split into two separate chromosomes (4 and 4A) in NGA and NAA. ...
Subjects: Evolutionary Biology. Contributor: Michael N. Romanov.
Interchromosomal rearrangements involving microchromosomes are rare events in birds. To date, they have been found mostly in Neognathae and Neoaves (e.g., Psittaciformes, Falconiformes, and Cuculiformes), although only a few orders have been analyzed. Hence, cytogenomic studies focusing on microchromosomes in species belonging to different bird orders are essential to shed more light on the avian chromosome and karyotype evolution. Relevant hypothetical Neognathae, Neoaves and other ancestral karyotypes can be reconstructed to trace these rearrangements. In a more recent study, a comparative chromosome mapping for chicken microchromosomes 10 to 28 was performed using interspecies BAC-based FISH hybridization in five species, representing four Neoaves orders (Caprimulgiformes, Piciformes, Suliformes, and Trogoniformes). These results suggest that the ancestral microchromosomal syntenies are conserved in Pteroglossus inscriptus (Piciformes), Ramphastos tucanus tucanus (Piciformes), and Trogon surrucura surrucura (Trogoniformes). On the other hand, chromosome reorganization in Phalacrocorax brasilianus (Suliformes) and Hydropsalis torquata (Caprimulgiformes) included fusions involving both macro-and microchromosomes. Fissions in macrochromosomes were observed in P. brasilianus and H. torquata. No interchromosomal rearrangement involving microchromosomes were found to be shared between avian orders where rearrangements were detected. These findings suggest that convergent evolution involving microchromosomal change is a rare event in birds and may be appropriate in cytotaxonomic inferences in orders where these rearrangements occurred. Keywords: avian cytogenomics, microchromosomes, evolution, genome organization, FISH, chromosomal rearrangements
... Genomic chromosomal rearrangement is likely to be an important source of gene loss events. Massive karyotype alterations have profoundly affected vertebrate evolution in general (Damas et al. 2021), as well as the evolution of certain crown lineages (Nanda et al. 2007;Harewood and Fraser 2014;Furo et al. 2018). Recent advances in genomic research have allowed thorough mapping of gene losses in a number of gene classes, including immune genes such as immune receptors, cytokines and other molecules directly affecting immune signalling (Wang et al. 2006;Temperley et al. 2008;Bainová et al. 2014;van der Loo et al. 2016;Velová et al. 2018). ...
... Thus, diversity in avian immune responses to peripheral stimulation remains largely unknown. Of particularly relevance to this issue is the investigation of immune response regulation in species with highly rearranged genomes, such as the parrots (Nanda et al. 2007;Furo et al. 2018). Therefore, here we focused on neuroinflammatory effects of LPS-induced peripheral inflammation in budgerigars, a model parrot species, where we revealed CNR2 pseudogenisation. ...
... We were able to identify putative remnants of the CNR2 pseudogene in the budgerigar genome, however, indicating apparent CNR2 pseudogenization following massive karyotype rearrangements early in parrot phylogeny (Nanda et al. 2007;Furo et al. 2018). Interestingly, a comparison of the karyotype localisation of passerine CNR2-neighbouring genes in the budgerigar and kakapo genomes suggested two presumably independent karyotype rearrangement events in parrots resulting in CNR2 loss. ...
In vertebrates, an ancient duplication in the genes for cannabinoid receptors (CNRs) allowed the evolution of specialised endocannabinoid receptors expressed in the brain (CNR1) and the periphery (CNR2). While dominantly conserved throughout vertebrate phylogeny, our comparative genomic analysis suggests that certain taxa may have lost either the CNR1 regulator of neural processes or, more frequently, the CNR2 involved in immune regulation. Focussing on conspicuous CNR2 pseudogenization in parrots (Psittaciformes), a diversified crown lineage of cognitively-advanced birds, we highlight possible functional effects of such a loss. Parrots appear to have lost the CNR2 gene at at least two separate occasions due to chromosomal rearrangement. Using gene expression data from the brain and periphery of birds with experimentally-induced sterile inflammation, we compare CNR and inflammatory marker (interleukin 1 beta, IL1B) expression patterns in CNR2-deficient parrots (represented by the budgerigar, Melopsittacus undulatus and five other parrot species) with CNR2-intact passerines (represented by the zebra finch, Taeniopygia guttata). Though no significant changes in CNR expression were observed in either parrots or passerines during inflammation of the brain or periphery, we detected a significant up-regulation of IL1B expression in the brain after stimulation with lipopolysaccharide (LPS) only in parrots. As our analysis failed to show evidence for selection on altered CNR1 functionality in parrots, compared to other birds, CNR1 is unlikely to be involved in compensation for CNR2 loss in modulation of the neuroimmune interaction. Thus, our results provide evidence for the functional importance of CNR2 pseudogenization for regulation of neuroinflammation.
... The introduction of new cytogenetic tools, especially comparative chromosome painting has helped to improve the understanding of karyotype evolution and phylogenetic relationships among different species of birds (Kretschmer et al., 2014(Kretschmer et al., , 2015(Kretschmer et al., , 2018aFuro et al., 2015Furo et al., , 2018Rodrigues et al., 2018). The variety of whole chromosome painting probes now available include chicken (Gallus gallus-GGA), stone-curlew (Burhinus oedicnemus-BOE), white hawk (Leucopternis albicollis-LAL), griffon vulture (Gyps fulvus-GFU) and eared dove (Zenaida auriculata-ZAU) (Nie et al., 2009;de Oliveira et al., 2010;Kretschmer et al., 2018b). ...
... There is an urgent need to use these new techniques to clarify the problems concerning avian karyotypes and phylogenetic relationships in a greater number of species (Dobigny et al., 2004;Furo et al., 2015Furo et al., , 2018Nie et al., 2015;Seligmann et al., 2019). The main aim of this study was to characterize the karyotype of G. melanops by classic cytogenetics, GGA chromosome painting probes and FISH with BACs selected from the genome library from microchromosomes of G. gallus in order to contribute to the phylogeny and karyotype evolution of the Rallidae family. ...
Although Rallidae is the most diverse family within Gruiformes, there is little information concerning the karyotype of the species in this group. In fact, Gallinula melanops, a species of Rallidae found in Brazil, is among the few species studied cytogenetically, but only with conventional staining and repetitive DNA mapping, showing 2n=80. Thus, in order to understand the karyotypic evolution and phylogeny of this group, the present study aimed to analyze the karyotype of G. melanops by classical and molecular cytogenetics, comparing the results with other species of Gruiformes. The results show that G. melanops has the same chromosome rearrangements as described in Gallinula chloropus (Clade Fulica), including fission of ancestral chromosomes 4 and 5 of Gallus gallus (GGA), beyond the fusion between two of segments resultants of the GGA4/GGA5, also fusions between the chromosomes GGA6/GGA7. Thus, despite the fact that some authors have suggested the inclusion of G. melanops in genus Porphyriops, our molecular cytogenetic results confirm its place in the Gallinula genus.
... Advances in molecular cytogenetics have shown that ancestral macrochromosomes have been highly rearranged in Psittaciformes (Nanda et al., 2007;Furo et al., 2015aFuro et al., , 2018. Hence, although chromosome painting with probes derived from chicken Gallus gallus (GGA) revealed three associations shared by all species of Psittaciformes analyzed so far -GGA1/4, GGA6/7, and GGA8/9 (Seabury et al., 2013;Furo et al., 2015aFuro et al., , 2018 -there are few chromosomal similarities shared between New World and Old World Psittaciformes. ...
... Advances in molecular cytogenetics have shown that ancestral macrochromosomes have been highly rearranged in Psittaciformes (Nanda et al., 2007;Furo et al., 2015aFuro et al., , 2018. Hence, although chromosome painting with probes derived from chicken Gallus gallus (GGA) revealed three associations shared by all species of Psittaciformes analyzed so far -GGA1/4, GGA6/7, and GGA8/9 (Seabury et al., 2013;Furo et al., 2015aFuro et al., , 2018 -there are few chromosomal similarities shared between New World and Old World Psittaciformes. ...
... Nevertheless, the results of GGA probes are limited as they do not detect most intrachromosomal rearrangements useful for phylogenetic inferences (Furo et al., 2015a,b;Furo et al., 2018;Kretschmer et al., 2018a). The use of probes from the white hawk (Leucopternis albicollis, LAL-2n = 66), with a highly derived karyotype involving multiple fissions on the ancestral chromosome (GGA1-GGA5) (de Oliveira et al., 2010), have enabled the detection of key intrachromosomal rearrangements (inversions, fissions), which together with noreciprocal translocations and tandem fusions represent the main types of mechanisms responsible for their karyotypical divergence (Furo et al., 2015a(Furo et al., , 2018. ...
Myiopsitta monachus is a small Neotropical parrot (Psittaciformes: Arini Tribe) from subtropical and temperate regions of South America. It has a diploid chromosome number 2n = 48, different from other members of the Arini Tribe that have usually 70 chromosomes. The species has the lowest 2n within the Arini Tribe. In this study, we combined comparative chromosome painting with probes generated from chromosomes of Gallus gallus and Leucopternis albicollis, and FISH with bacterial artificial chromosomes (BACs) selected from the genome library of G. gallus with the aim to shed light on the dynamics of genome reorganization in M. monachus in the phylogenetic context. The homology maps showed a great number of fissions in macrochromosomes, and many fusions between microchromosomes and fragments of macrochromosomes. Our phylogenetic analysis by Maximum Parsimony agree with molecular data, placing M. monachus in a basal position within the Arini Tribe, together with Amazona aestiva (short tailed species). In M. monachus many chromosome rearrangements were found to represent autopomorphic characters, indicating that after this species split as an independent branch, an intensive karyotype reorganization took place. In addition, our results show that M. monachus probes generated by flow cytometry provide novel cytogenetic tools for the detection of avian chromosome rearrangements, since this species presents breakpoints that have not been described in other species.
... The advances in comparative chromosome mapping with the use of chromosome painting has provided important information for inferences about phylogenetic relationships in some groups of birds, clarifying some problems left by the analyses of molecular biology [9][10][11][12][13][14]. Furthermore, despite the apparent karyotypical conservation among birds observed by conventional staining, comparative chromosome painting has revealed many rearrangements, such as fusions and fissions in several macrochromosomes; this information allowed the inference of a putative ancestral karyotype (PAK) of birds, which is actually highly similar to the chromosomal complement of Gallus gallus, with the exception of pair 4, which corresponds to two distinct pairs in the proposed ancestral karyotype [9][10][11]15,16]. ...
... The advances in comparative chromosome mapping with the use of chromosome painting has provided important information for inferences about phylogenetic relationships in some groups of birds, clarifying some problems left by the analyses of molecular biology [9][10][11][12][13][14]. Furthermore, despite the apparent karyotypical conservation among birds observed by conventional staining, comparative chromosome painting has revealed many rearrangements, such as fusions and fissions in several macrochromosomes; this information allowed the inference of a putative ancestral karyotype (PAK) of birds, which is actually highly similar to the chromosomal complement of Gallus gallus, with the exception of pair 4, which corresponds to two distinct pairs in the proposed ancestral karyotype [9][10][11]15,16]. ...
... viridis); however, it is absent in A. cajaneus ( Table 1). The association between GGA6/GGA7 has been detected in five species belonging to different orders of birds: Galliformes-Numida meleagris [21], Strigiformes-Pulsatrix perspicillata [22], Trogoniformes-Trogon s. surrucura [23], Psittaciformes-Nymphicus hollandicus, Agapornis roseicollis, Melopsittacus undulates [24], Ara macao [25], Ara chloropterus, Anodorhynchus hyacinthinus [9], Psittacus erithacus [26], Pyrrhura frontalis, Amazona aestiva [11] and Columbiformes-Leptotila verreauxi [16]. Hence, GGA6/GGA7 association originated independently in five different orders. ...
Gruiformes is a group with phylogenetic issues. Recent studies based on mitochondrial and genomic DNA have proposed the existence of a core Gruiformes, consisting of five families: Heliornithidae, Aramidae, Gruidae, Psophiidae and Rallidae. Karyotype studies on these species are still scarce, either by conventional staining or molecular cytogenetics. Due to this, this study aimed to analyze the karyotype of two species (Aramides cajaneus and Psophia viridis) belonging to families Rallidae and Psopiidae, respectively, by comparative chromosome painting. The results show that some chromosome rearrangements in this group have different origins, such as the association of GGA5/GGA7 in A. cajaneus, as well as the fission of GGA4p and association GGA6/GGA7, which place P. viridis close to Fulica atra and Gallinula chloropus. In addition, we conclude that the common ancestor of the core Gruiformes maintained the original syntenic groups found in the putative avian ancestral karyotype.
... Most orders of birds show no change from the microchromosomal pattern seen in chicken, conserving a pattern of organization at both karyotypic and microsynteny level across Aves for over 150 million years [Zhang et al., 2014;O'Connor et al., 2019]. Nevertheless, despite the fact that this successful organization might be favored by natural selection in the avian class [O'Connor et al., 2018[O'Connor et al., , 2019Zhang, 2018], there are well-documented exceptions to this rule, such as Accipitriformes, Falconiformes, and Psittaciformes [de Oliveira et al., 2005[de Oliveira et al., , 2010[de Oliveira et al., , 2013Nishida-Umehara et al., 2007;Furo et al., 2015aFuro et al., , 2017Furo et al., , 2018. In this sense, Ciconiidae is a group to be added to this list of birds which have broken this genome stability. ...
Despite the variation observed in the diploid chromosome number of storks (Ciconiiformes, Ciconiidae), from 2n = 52 to 2n = 78, most reports have relied solely on analyses by conventional staining. As most species have similar macrochromosomes, some authors propose that karyotype evolution involves mainly fusions between microchromosomes, which are highly variable in species with different diploid numbers. In order to verify this hypothesis, in this study, the karyotypes of 2 species of storks from South America with different diploid numbers, the jabiru (Jabiru mycteria, 2n = 56) and the maguary stork (Ciconia maguary, 2n = 72), were analyzed by chromosome painting using whole chromosome probes from the macrochromosomes of Gallus gallus (GGA) and Leucopternis albicollis (LAL). The results revealed that J. mycteria and C. maguary share synteny within chromosome pairs 1-9 and Z. The syntenies to the macrochromosomes of G. gallus are conserved, except for GGA4, which is homologous to 2 different pairs, as in most species of birds. A fusion of GGA8 and GGA9 was observed in both species. Additionally, chromosomes corresponding to GGA4p and GGA6 are fused to other segments that did not hybridize to any of the macrochromosome probes used, suggesting that these segments correspond to microchromosomes. Hence, our data corroborate the proposed hypothesis that karyotype evolution is based on fusions involving microchromosomes. In view of the morphological constancy of the macrochromosome pairs in most Ciconiidae, we propose a putative ancestral karyotype for the family, including the GGA8/GGA9 fusion, and a diploid number of 2n = 78. The use of probes for microchromosome pairs should be the next step in identifying other synapomorphies that may help to clarify the phylogeny of this family.
Birds (Aves) are the most speciose of terrestrial vertebrates, displaying Class-specific characteristics yet incredible external phenotypic diversity. Critical to agriculture and as model organisms, birds have adapted to many habitats. The only extant examples of dinosaurs, birds emerged ~150 mya and >10% are currently threatened with extinction. This review is a comprehensive overview of avian genome ("chromosomic") organization research based mostly on chromosome painting and BAC-based studies. We discuss traditional and contemporary tools for reliably generating chromosome-level assemblies and analyzing multiple species at a higher resolution and wider phylogenetic distance than previously possible. These results permit more detailed investigations into inter- and intrachromosomal rearrangements, providing unique insights into evolution and speciation mechanisms. The 'signature' avian karyotype likely arose~250 mya and remained largely unchanged in most groups including extinct dinosaurs. Exceptions include Psittaciformes, Falconiformes, Caprimulgiformes, Cuculiformes, Suliformes, occasional Passeriformes, Ciconiiformes, and Pelecaniformes. The reasons for this remarkable conservation may be the greater diploid chromosome number generating variation (the driver of natural selection) through a greater possible combination of gametes and/or an increase in recombination rate. A deeper understanding of avian genomic structure permits the exploration of fundamental biological questions pertaining to the role of evolutionary breakpoint regions and homologous synteny blocks.
The reed warbler (Acrocephalus scirpaceus) is a long-distance migrant passerine with a wide distribution across Eurasia. This species has fascinated researchers for decades, especially its role as host of a brood parasite, and its capacity for rapid phenotypic change in the face of climate change. Currently, it is expanding its range northwards in Europe, and is altering its migratory behaviour in certain areas. Thus, there is great potential to discover signs of recent evolution and its impact on the genomic composition of the reed warbler. Here we present a high-quality reference genome for the reed warbler, based on PacBio, 10X and Hi-C sequencing. The genome has an assembly size of 1,075,083,815 bp with a scaffold N50 of 74,438,198 bp and a contig N50 of 12,742,779 bp. BUSCO analysis using aves_odb10 as a model showed that 95.7% of BUSCO genes were complete. We found unequivocal evidence of two separate macrochromosomal fusions in the reed warbler genome, in addition to the previously identified fusion between chromosome Z and a part of chromosome 4A in the Sylvioidea superfamily. We annotated 14,645 protein-coding genes, and a BUSCO analysis of the protein sequences indicated 97.5% completeness. This reference genome will serve as an important resource, and will provide new insights into the genomic effects of evolutionary drivers such as coevolution, range expansion, and adaptations to climate change, as well as chromosomal rearrangements in birds.
Interchromosomal rearrangements involving microchromosomes are rare events in birds. To date, they have been found mostly in Psittaciformes, Falconiformes, and Cuculiformes, although only a few orders have been analyzed. Hence, cytogenomic studies focusing on microchromosomes in species belonging to different bird orders are essential to shed more light on the avian chromosome and karyotype evolution. Based on this, we performed a comparative chromosome mapping for chicken microchromosomes 10 to 28 using interspecies BAC-based FISH hybridization in five species, representing four Neoaves orders (Caprimulgiformes, Piciformes, Suliformes, and Trogoniformes). Our results suggest that the ancestral microchromosomal syntenies are conserved in Pteroglossus inscriptus (Piciformes), Ramphastos tucanus tucanus (Piciformes), and Trogon surrucura surrucura (Trogoniformes). On the other hand, chromosome reorganization in Phalacrocorax brasilianus (Suliformes) and Hydropsalis torquata (Caprimulgiformes) included fusions involving both macro- and microchromosomes. Fissions in macrochromosomes were observed in P. brasilianus and H. torquata. Relevant hypothetical Neognathae and Neoaves ancestral karyotypes were reconstructed to trace these rearrangements. We found no interchromosomal rearrangement involving microchromosomes to be shared between avian orders where rearrangements were detected. Our findings suggest that convergent evolution involving microchromosomal change is a rare event in birds and may be appropriate in cytotaxonomic inferences in orders where these rearrangements occurred.
