Chromosome evolution in birds: molecular cytogenetics, comparative genomics and whole genome assemblies

Contemporary iterations of avian phylogenies based on multiple genome sequence assemblies assign three major clades: Palaeognathae (mostly ratite birds), Galloanseres (land and waterfowl) and the largest group—Neoaves. The latter two are sister clades representing subdivisions of Neognathae, while Neoaves further subdivide into Columbaves (pigeons/doves/cuckoos/bustards, etc.), Mirandornithes (flamingos/grebes), Telluraves (“higher land birds”, including finches) and the newly recognized Elementaves (e.g., penguins/pelicans/hummingbirds/swifts/cranes/shorebirds). Molecular studies provide clade information, likely divergence timings and a framework from which gross genomic (chromosomal) changes may be mapped. In this review, we consider the patterns of chromosome change that have occurred throughout all avian clades thus far examined, citing studies from standard karyotyping through molecular cytogenetics to whole genome assemblies. Standard karyotyping led to the realization that most chromosomes (particularly the microchromosomes and dot chromosomes) could not be distinguished by classical means. Indeed, cross-species comparisons were difficult, even among the macrochromosomes, because of indistinct banding patterns. Based on fluorescence (or fluorescent) in situ hybridization (FISH), comparative genomics was thence progressed considerably by cross-species chromosome painting (Zoo-FISH) for the macrochromosomes and interspecific mapping of bacterial artificial chromosome (BAC) probes for the microchromosomes. A key finding was that the most studied species, the chicken, fortuitously, has a genomic organization somewhat akin to that of the ancestral karyotype and tends to be the standard from which all others are measured. A notable exception is the fusion of basal chromosome 4 with a smaller chromosome that convergently appears in some other Galliformes, at least one goose and one dove species. While some groups such as Falconiformes (falcons, etc.) and Psittaciformes (parrots, etc.) underwent extensive interchromosomal change, most, broadly speaking, retain a basic karyotype that differs little from bird to bird. Many, e.g., Passeriformes (finches, songbirds, etc.) and Columbiformes (pigeons, doves), do this despite multiple intrachromosomal rearrangements. The complete karyotype and fully established chromosome-level genome assembly of the chicken allow full integration of DNA sequence assembly with karyotype. They further permit cytogenetic studies to be performed using genome assemblies alone alongside cutting-edge long-read sequencing and optical mapping without the need for chromosome preparation. The classic ZW sex-determination system of birds is easily visible in most Neognathae species, but intrachromosomal change in the sex chromosomes is faster than in the autosomes; indeed, there are numerous examples of autosomal fusions and new sex chromosomes formed. Sex chromosomes aside, the classic avian karyotype represents a very successful mode of genome organization established before the emergence of the dinosaurs and perpetuated to this day in their only living descendants.