A Bird's-Eye View of Chromosomic Evolution in the Class Aves

Abstract

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.

Keywords: avian genome; avian karyotype; interchromosomal rearrangements; intrachromosomal rearrangements; macrochromosomes; microchromosomes.

Figure 1

Ideogram view in the NCBI Genome Data Viewer for two chicken (Gallus gallus, GGA) representative genome assemblies. (a) The previous assembly GRCg6a (GCF_000002315.6) released on 27 March 2018 with 1 to 33 autosomes. (b) The latest assembly bGalGal1.mat.broiler.GRCg7b (GCF_016699485.2) as of 19 January 2021 has 1 to 39 autosomes (including macrochromosomes GGA1–GGA9 and microchromosomes GGA10–GGA39) and fewer unplaced scaffolds as a result of work later published in Huang et al. [133]; Z and W, sex chromosomes; MT, mitochondrial genome.

Figure 2

Example of dual FISH results for chicken (Gallus gallus—GGA) chromosome 12 to confirm correct mapping. The p-arm BAC (CH261-88K1) is labelled with FITC (fluorescein isothiocyanate) (green) and the q-arm BAC (CH261-152H14) is labelled with Texas Red (red). Scale bar 10 μm.

Figure 3

Microchromosomal conservation observed across a wide range of avian species as revealed by testing BACs from chicken chromosome 24 (CH261-103F4 FITC in green and CH261-65O4 Texas Red in red): Phalacrocorax brasilianus (a), Crotophaga ani (b), and Geotrygon montana (c). Frame enlargements immediately beneath, occasional multiple signals (e.g., in (b,c)) as commonplace in FISH experiments and representing small amounts of background hybridization.

Figure 4

Bird phylogeny illustrating the presence or lack of interchromosomal rearrangement involving microchromosomes based on BAC FISH. The numbers of species with or without interchromosomal rearrangement involving microchromosomes is illustrated in each order. Macrochromosomal fusions are not listed. Phylogenetic relationships followed Jarvis et al. [16]. Light colored boxes indicate where interchromosomal changes occurred.

Figure 5

Hybridization of GGA22 BACs (CH261-40J9-FITC in green and CH261-18G17-Texas Red in red) to monk parakeet (Myiopsitta monachus, MMO) metaphase illustrating fusion of the ancestral microchromosome to a macrochromosome.

Figure 6

Ideogram representing karyotypic structure of the cockatiel (Nymphus hollandicus, NHO) illustrating an overall structure. Each chicken (GGA) homolog is represented as a different color.

Figure 7

Hybridization of GGA18 BACs (CH261-60N6-FITC in green and CH261-72B18-Texas Red in red) to peregrine falcon (Falco peregrinus) metaphases illustrating fusion of ancestral microchromosome to a macrochromosome. Scale bar 10 μm.

Figure 8

Ideogram representing overall karyotypic structure of the peregrine falcon (Falco peregrinus—FPE) illustrating an extensive amount of interchromosomal rearrangement throughout the karyotype. Each chicken (GGA) homolog is represented as a different color.