Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots

Abstract

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.

Fig. 1. Phylogeny and comparative genomics of parrots.

a The phylogeny of nine bird species shows the divergence time (denoted at the nodes) calibrated with fossil records at the node Psittacopasserae (51.81–66.5 My) and Strigopoidea (15.9–66.5 My). The orange asterisks to the left of species names indicate the availability of chromosome-level assemblies. The numbers of gene gains (0, in red) and losses (74, in blue) were denoted at the Psittaciformes node. The vertical bars show the frequency of TE (LTR and CR1) insertions during the evolution of bird species (see details in “Methods”). CR1 is divided into CR1-psi and the other CR1. CR1-psi originated in parrots and continued to propagate in parrot lineages. The numbers of diploid chromosomes are listed in the right panel that shows greater variation in parrots. b, c The loss of ALC1 and PARP3 (highlighted in black) in parrots. Monk parakeet is used to represent the parrot lineage. The synteny of genes around ALC1 and PARP3 is illustrated by gray bands connecting orthologs across species. ALC1 was pseudogenized (indicated by dashed rectangle) due to multiple exon losses (Supplementary Fig. S6). Multiple copies of CR1-psi have been inserted at the ALC1 locus. Parrots have evolved an inversion around the PARP3 locus and inversion breakpoint co-localize with PARP3. Illustrations reproduced by permission of Lynx Edicions.

Fig. 2. Frequent chromosomal rearrangements across parrot genomes.

Pairwise whole-genome alignments across eight chromosome-level assemblies of bird genomes. Each horizontal bar represents one chromosome, and chromosome IDs of chicken were labeled at the bottom; for parrot genomes some chromosomes were renamed following chromosome fissions. Chromosomes that experienced recurrent chromosomal rearrangements are highlighted in colors. Chromosome 11 and 25 are highlighted in color which were fused to the sex chromosome in monk parakeet. Illustrations reproduced by permission of Lynx Edicions.

Fig. 3. The Evolutionary history of parrot sex chromosomes.

a The Hi-C contact map of chromosomes that are homologous to chicken chr11, chr25, and chrZ. The three chromosomes are presented in three chromosome territories in chicken, but only one in monk parakeet and two in blue-fronted amazon. b The FISH images for the probes of chicken chr11 hybridization in monk parakeet. The FISH result for chicken chr25 probe is shown in the Supplementary Fig. S10. c The female sequencing coverage for the chromosomes homologous to chicken chr11, chr25, and chrZ. In monk parakeet the blue-fronted amazon the coverage of the part of chrZ homologous to chicken chr11 is reduced by half, compared to PARs or autosomes. d Sequence divergence of the Z and W chromosome reveals the pattern of evolutionary strata. Each dot represents a 100-kb sliding window along the Z chromosome. The S0 and S1 were defined based on the homology of Neoaves S0 and S1 (Xu, Auer et al. 2019). Songbirds (right panel) have four evolutionary strata and parrots (left) have a similar stratum pattern but have one additional stratum (S4) due to the fusion of chr11. e Phylogeny of the Z-W gametologs for a S3 (left panel) and a S4 (right) gametologous gene. Parrot Z- and W-linked gametologs are clustered together respectively, and share a common ancestor, suggesting common origins of S3 and S4 in parrots. Additional gene trees are given in the Supplementary Fig. S13. f A schematic diagram depicting the evolutionary history of sex chromosomes since the common ancestor of songbirds and parrots. Whether chr25 has been added to the chrW remains to be verified. Illustrations reproduced by permission of Lynx Edicions.

Fig. 4. Non-adaptive evolution of the neo-sex chromosome.

a A heatmap showing the expression (measured by log (1+TPM)) of Z-W gene pairs across male and female tissues in monk parakeet. Each row represents one gene. The top three panels annotate whether a gene is Z- or W-linked and in which tissue/sex it is expressed. The left panel annotates which stratum a gene belongs to. The W-linked gametologs are present only in females (purple in male), but their expression profiles are similar to their Z-linked homologs. b The X- and Y-axis show the expression of Z- and W-linked gametologs, respectively. The solid line represents the regression relation between the expression of the Z and W, while the dashed line indicates the situation of equal Z-W expression. c Male/female expression for Z-linked genes on the both old (n = 529) and new (n = 122) sex chromosomes, as well as autosomal genes (n = 7,562). The boxplots show the first quartile, median, and third quartile values. d Temporal dynamics of TE content on the monk parakeet W chromosome divided into five evolutionary strata. LTRs are more abundant in younger strata.