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The karyotype of most birds has remained considerably stable during more than 100 million years’ evolution, except for some groups, such as parrots. The evolutionary processes and underlying genetic mechanism of chromosomal rearrangements in parrots, however, are poorly understood. Here, using chromosome-level assemblies of four parrot genomes, we uncover frequent chromosome fusions and fissions, with most of them occurring independently among lineages. The increased activities of chromosomal rearrangements in parrots are likely associated with parrot-specific loss of two genes, ALC1 and PARP3 , that have known functions in the repair of double-strand breaks and maintenance of genome stability. We further find that the fusion of the ZW sex chromosomes and chromosome 11 has created a pair of neo-sex chromosomes in the ancestor of parrots, and the chromosome 25 has been further added to the sex chromosomes in monk parakeet. Together, the combination of our genomic and cytogenetic analyses characterizes the complex evolutionary history of chromosomal rearrangements and sex chromosomes in parrots. Parrots have undergone substantial karyotype evolution compared to most other birds. Here, Huang et al. analyze chromosome-level genome assemblies for four parrot species and elucidate the complex evolutionary history of parrot chromosomes.

The information contained in population genomic data can tell us much about the past ecology and evolution of species. We leveraged detailed phenotypic and genomic data of nearly all living kākāpō to understand the evolution of its feather color polymorphism. The kākāpō is an endangered and culturally significant parrot endemic to Aotearoa New Zealand, and the green and olive feather colorations are present at similar frequencies in the population. The presence of such a neatly balanced color polymorphism is remarkable because the entire population currently numbers less than 250 birds, which means it has been exposed to severe genetic drift. We dissected the color phenotype, demonstrating that the two colors differ in their light reflectance patterns due to differential feather structure. We used quantitative genomics methods to identify two genetic variants whose epistatic interaction can fully explain the species’ color phenotype. Our genomic forward simulations show that balancing selection might have been pivotal to establish the polymorphism in the ancestrally large population, and to maintain it during population declines that involved a severe bottleneck. We hypothesize that an extinct apex predator was the likely agent of balancing selection, making the color polymorphism in the kākāpō a “ghost of selection past.”

The relationships of passerines (such as the well-studied zebra finch) with non-passerine birds is one of the great enigmas of avian phylogenetic research, because decades of extensive morphological and molecular studies yielded highly inconsistent results between and within data sets. Here we show the first application of the virtually homoplasy-free retroposon insertions to this controversy. Our study examined ~200,000 retroposon-containing loci from various avian genomes and retrieved 51 markers resolving early bird phylogeny. Among these, we obtained statistically significant evidence that parrots are the closest and falcons the second-closest relatives of passerines, together constituting the Psittacopasserae and the Eufalconimorphae, respectively. Our new and robust phylogenetic framework has substantial implications for the interpretation of various conclusions drawn from passerines as model organisms. This includes insights of relevance to human neuroscience, as vocal learning (that is, birdsong) probably evolved in the psittacopasseran ancestor, >30 million years earlier than previously assumed. Zebra finches are passerine birds, but their phylogenetic relationship with non-passerine birds remains controversial. By examining retroposon insertion loci in avian genomes, the authors reveal that parrots are the closest relatives of passerines, which may have implications for understanding the evolution of birdsong.

Vibrant feathers from Amazonian parrots were among the most prestigious symbols of status in the pre-Hispanic Andes, yet their acquisition required traversing the formidable Andean mountain range. Here, we investigate feathers recovered from an intact, elite masonry tomb at the coastal religious center of Pachacamac, associated with the pre-Inca Ychsma culture that flourished during the Late Intermediate Period (ca. 1000–1470 CE). By integrating ancient DNA, stable isotope analysis, and spatial modeling, we reconstruct the complete journey of these feathers. Genomic data identify four distinct Amazonian parrot species ( Ara macao , A. ararauna , A. chloropterus , Amazona farinosa ) and reveal high genetic diversity, indicating extraction from wild populations rather than local breeding. Stable carbon and nitrogen isotope analysis reveals that these birds consumed a C4-rich coastal diet, demonstrating they were transported alive across the Andes and kept in the arid coast. Finally, we identify specific trans-Andean corridors used for this exchange by combining species distribution models of ancient habitats with landscape resistance modeling. Our findings reveal a sophisticated, managed trade network operated by the Ychsma through intermediaries, challenging views of pre-Inca regionalism and establishing a multidisciplinary toolkit for tracing ancient exchange. Here, the authors combine ancient DNA, stable isotopes, and computational modeling to study colorful feathers from a pre-Incan tomb in Peru. They identify four species of parrots, which were likely captured in the Amazon before being transported across the Andes before being fed a local, coastal diet.

The study of hybrid zones advances understanding of the speciation process, and approaches incorporating genomic data are increasingly used to draw significant conclusions about the impact of hybridisation. Despite the progress made, the complex interplay of factors that can lead to substantially variable hybridisation outcomes are still not well understood, and many systems and/or groups remain comparatively poorly studied. Our study aims to broaden the literature on avian hybrid zones, investigating a potentially geographically and temporally complex putative hybrid zone between two native Australian non-sister parrot species, the pale-headed and eastern rosellas (Platycercus adscitus and Platycercus eximius, respectively). We analysed six plumage traits and >1400 RADseq loci and detected hybrid individuals and an unexpectedly complex geographic structure. The hybrid zone is larger than previously described due to either observer bias or its movement over recent decades. It comprises different subregions where genetic and plumage signals of admixture vary markedly in their concordance. Evidence of contemporary hybridisation (later generation and backcrossed individuals) both within and beyond the previously defined zone, when coupled with a lack of F1 hybrids and differential patterns of introgression among potentially diagnostic loci, indicates a lack of post-zygotic barriers to gene flow between species. Despite ongoing gene flow, species boundaries are likely maintained largely by strong pre-mating barriers. These findings are discussed in detail and future avenues for research into this system are proposed, which would be of benefit to the speciation and hybrid zone literature.

Telomeres, the caps of eukaryotic chromosomes, control chromosome stability and cellular senescence, but aging and exposure to chronic stress are suspected to cause attrition of telomere length. We investigated the effect of social isolation on telomere length in the highly social and intelligent African Grey parrot (Psittacus erithacus erithacus). Our study population consisted of single-housed (n = 26) and pair-housed (n = 19) captive individuals between 0.75 to 45 years of age. Relative telomere length of erythrocyte DNA was measured by quantitative real-time PCR. We found that telomere length declined with age (p<0.001), and socially isolated parrots had significantly shorter telomeres compared to pair-housed birds (p<0.001) - even among birds of similar ages. Our findings provide the first evidence that social isolation affects telomere length, which supports the hypothesis that telomeres provide a biomarker indicating exposure to chronic stress.

Background Conures are a morphologically diverse group of Neotropical parrots classified as members of the tribe Arini , which has recently been subjected to a taxonomic revision. The previously broadly defined Aratinga genus of this tribe has been split into the ‘true’ Aratinga and three additional genera, Eupsittula , Psittacara and Thectocercus . Popular markers used in the reconstruction of the parrots’ phylogenies derive from mitochondrial DNA. However, current phylogenetic analyses seem to indicate conflicting relationships between Aratinga and other conures, and also among other Arini members. Therefore, it is not clear if the mtDNA phylogenies can reliably define the species tree. The inconsistencies may result from the variable evolution rate of the markers used or their weak phylogenetic signal. To resolve these controversies and to assess to what extent the phylogenetic relationships in the tribe Arini can be inferred from mitochondrial genomes, we compared representative Arini mitogenomes as well as examined the usefulness of the individual mitochondrial markers and the efficiency of various phylogenetic methods. Results Single molecular markers produced inconsistent tree topologies, while different methods offered various topologies even for the same marker. A significant disagreement in these tree topologies occurred for cytb , nd2 and nd6 genes, which are commonly used in parrot phylogenies. The strongest phylogenetic signal was found in the control region and RNA genes. However, these markers cannot be used alone in inferring Arini phylogenies because they do not provide fully resolved trees. The most reliable phylogeny of the parrots under study is obtained only on the concatenated set of all mitochondrial markers. The analyses established significantly resolved relationships within the former Aratinga representatives and the main genera of the tribe Arini . Such mtDNA phylogeny can be in agreement with the species tree, owing to its match with synapomorphic features in plumage colouration. Conclusions Phylogenetic relationships inferred from single mitochondrial markers can be incorrect and contradictory. Therefore, such phylogenies should be considered with caution. Reliable results can be produced by concatenated sets of all or at least the majority of mitochondrial genes and the control region. The results advance a new view on the relationships among the main genera of Arini and resolve the inconsistencies between the taxa that were previously classified as the broadly defined genus Aratinga . Although gene and species trees do not always have to be consistent, the mtDNA phylogenies for Arini can reflect the species tree.

Genetic diversity at community, population and individual levels is thought to influence the spread of infectious disease. At the individual level, inbreeding and heterozygosity are associated with increased risk of infection and disease severity. Host genotype rarity may also reduce infection risk if pathogens are co-adapted to common or local hosts, but to date, no studies have investigated the relative importance of genotype rarity and heterozygosity for infection in a wild, sexually reproducing vertebrate. With beak and feather disease virus (BFDV) infection in a wild parrot ( Platycercus elegans ), we show that both heterozygosity and genotype rarity of individual hosts predicted infection, but in contrasting ways. Heterozygosity was negatively associated with probability of infection, but not with infection load. In contrast, increased host genotype rarity was associated with lower viral load in infected individuals, but did not predict infection probability. These effects were largely consistent across subspecies, but were not evident at the population level. Subspecies and age were also strongly associated with infection. Our study provides novel insights into infection dynamics by quantifying rarity and diversity simultaneously. We elucidate roles that host genetic diversity can play in infection dynamics, with implications for understanding population divergence, intraspecific diversity and conservation.

The mechanisms underlying the taxonomic assembly of montane biotas are still poorly understood. Most hypotheses have assumed that the diversification of montane biotas is loosely coupled to Earth history and have emphasized instead the importance of multiple long-distance dispersal events and biotic interactions, particularly competition, for structuring the taxonomic composition and distribution of montane biotic elements. Here we use phylogenetic and biogeographic analyses of species in the parrot genus Pionus to demonstrate that standing diversity within montane lineages is directly attributable to events of Earth history. Phylogenetic relationships confirm three independent biogeographic disjunctions between montane lineages, on one hand, and lowland dry-forest/wet-forest lineages on the other. Temporal estimates of lineage diversification are consistent with the interpretation that the three lineages were transported passively to high elevations by mountain building, and that subsequent diversification within the Andes was driven primarily by Pleistocene climatic oscillations and their large-scale effects on habitat change. These results support a mechanistic link between diversification and Earth history and have general implications for explaining high altitudinal disjuncts and the origin of montane biotas.

Data deposition to NCBI Genomes: This Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession AMXX00000000 (SMACv1.0, unscaffolded genome assembly). The version described in this paper is the first version (AMXX01000000). The scaffolded assembly (SMACv1.1) has been deposited at DDBJ/EMBL/GenBank under the accession AOUJ00000000, and is also the first version (AOUJ01000000). Strong biological interest in traits such as the acquisition and utilization of speech, cognitive abilities, and longevity catalyzed the utilization of two next-generation sequencing platforms to provide the first-draft de novo genome assembly for the large, new world parrot Ara macao (Scarlet Macaw). Despite the challenges associated with genome assembly for an outbred avian species, including 951,507 high-quality putative single nucleotide polymorphisms, the final genome assembly (>1.035 Gb) includes more than 997 Mb of unambiguous sequence data (excluding N's). Cytogenetic analyses including ZooFISH revealed complex rearrangements associated with two scarlet macaw macrochromosomes (AMA6, AMA7), which supports the hypothesis that translocations, fusions, and intragenomic rearrangements are key factors associated with karyotype evolution among parrots. In silico annotation of the scarlet macaw genome provided robust evidence for 14,405 nuclear gene annotation models, their predicted transcripts and proteins, and a complete mitochondrial genome. Comparative analyses involving the scarlet macaw, chicken, and zebra finch genomes revealed high levels of nucleotide-based conservation as well as evidence for overall genome stability among the three highly divergent species. Application of a new whole-genome analysis of divergence involving all three species yielded prioritized candidate genes and noncoding regions for parrot traits of interest (i.e., speech, intelligence, longevity) which were independently supported by the results of previous human GWAS studies. We also observed evidence for genes and noncoding loci that displayed extreme conservation across the three avian lineages, thereby reflecting their likely biological and developmental importance among birds.