Bizarre parrot chromosomes

Analyzing four chromosome-level genomes of parrots, we were surprised by the evolutionary dynamics of parrot (sex) chromosomes.

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I have been working on avian genomics since 10 years ago, but never thought bird chromosomes can be as dynamic as what we recently found in parrots. In general, bird karyotypes are extremely conserved, typically having ~10 pairs of macrochromosomes and ~30 pairs of microchromosomes. In 2017, I read a paper by Furo et al. on the study of monk parakeet karyotype which blew my mind. I was excited to know that some parrots can have a chromosome number as low as 24 (2n=48), and the W chromosome which is typically tiny in birds can be as large as the Z chromosome.

Fortunately, monk parakeets have been widely bred as a pet, thus no need to catch wild individuals for genome sequencing. In fact, monk parakeets have become invasive species in Europe and many other places. We decided to use PacBio long-reads to assemble a female genome of monk parakeet, hoping the repetitive W chromosome can be sequenced through.

Figure 1. A monk parakeet (Myiopsitta monachus). Photo by Yinghui Chen.

To our surprise, the sex chromosomes were more complex than we thought. We expected that many fusion events must have occurred in parrots, but did not realize that the sex chromosomes thought to be conserved also experienced fusions. The entire chromosome 11 was added to the ZW chromosomes of all parrots, and chromosome 25 was additionally added to sex chromosomes in monk parakeets. 

Figure 2. The evolutionary history of parrot sex chromosomes.

What can be possible causes for the drastic chromosomal rearrangements in parrots? To address that, we compared four parrots and a few other birds for both coding and noncoding parts of the genomes. Apparently, parrots have one active transposable element, termed CR1-psi, that has been propagating during parrot diversification. The insertions of CR1-psi seem to have mediated the loss of a conserved gene ALC1 which plays a role in DNA repair. Apart from that, the loss of another genome-stabilizing gene, PARP3, likely also contributed to the frequent chromosomal rearrangements in parrots.

Though we were only able to assemble a part of the W chromosome, the sequencing data of both sexes, as well as FISH (Fluorescence in situ hybridization) experiments, clearly demonstrated the role of a 21-bp satellite DNA in driving the expansion of the W chromosome of monk parakeet. As I wrote in the response letter to reviewers:

“We believe the present work sets an exciting example where genomic and cytogenetic methods complement each other and address scientific questions that are difficult to be addressed with genomic or cytogenetic tools alone, and we predict combining genomics and cytogenetics will be a new norm in future studies of karyotype evolution.“

References:

Furo, I. et al. Chromosomal mapping of repetitive DNAs in Myiopsitta monachus and Amazona aestiva (Psittaciformes, Psittacidae) with emphasis on the sex chromosomes. Cytogenet. Genome Res. 151, 151–160 (2017).

Huang, Z. et al. Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots. Nat Commun 13, 944 (2022). https://doi.org/10.1038/s41467-022-28585-1

Luohao Xu

Professor, Southwest University