Avian Cytogenomics: Small Chromosomes, Long Evolutionary History

Abstract

This review considers fundamental issues related to the genomics of birds (Aves), including the special organization and evolution of their chromosomes. In particular, we address the capabilities of molecular genetic/genomic approaches to clarify aspects of their evolutionary history, including how they have adapted to multiple habitats. We contemplate general genomic organization, including the small size and typical number of micro/macrochromosomes. We discuss recent genome sequencing efforts and how this relates to cytogenomic studies. We consider the emergence of this unique organization ~245 million years ago, examining examples where the "norm" is not followed. We address the functional role of synteny disruptions, centromere repositioning, repetitive elements, evolutionary breakpoints, synteny blocks and the role of the unique ZW sex chromosome system. By analyzing the cytogenetic maps and chromosomal rearrangements of eight species, the possibility of successfully applying modern genomic methods/technologies to identify general and specific features of genomic organization and an in-depth understanding of the fundamental patterns of the evolution of avian genomes are demonstrated. An interpretation of the observed genomic "variadicity" and specific chromosomal rearrangements is subsequently proposed. We also present a mathematical assessment of cross-species bacterial artificial chromosome (BAC) hybridization during genomic mapping in the white-throated sparrow, a species considered a key model of avian behavior. Building on model species (e.g., chicken), avian cytogenomics now encompasses hundreds of genomes across nearly all families, revealing remarkable genomic conservation with many dynamic aspects. Combining classical cytogenetics, high-throughput sequencing and emerging technologies provides increasingly detailed insights into the structure, function and evolutionary organization of these remarkable genomes.

Keywords: adaptation; avian genomes; birds (Aves); chromosomal rearrangements; chromosomes; cytogenomics; genome evolution; genome organization; genomic technologies; molecular genetic approaches.

Figure 1

Phylogeny and divergence times of birds and their ancestors (adapted and modified from [3,64]). The time scale is given in million years ago (MYA).

Figure 2

Vertebrate phylogeny and modes of sex determination in different taxa (adapted and modified from [132]). Red and black represent genetic sex determination with female and male heterogamety, respectively, whereas green corresponds to temperature-dependent sex determination. Birds and snakes have female heterogamety (albeit with sex chromosomes indistinguishable in the Palaeognathae), mammals have male heterogamety and other groups have different combinations.

Figure 3

Phylogenetic tree for eight neognaths [17]: canary (A), blackbird (B), pigeon (P), houbara (H), woodcock (W), chicken (C), guineafowl (G) and duck (D). The hypothetical ancestor of Neognathae is circled in red. The ostrich (O), a representative of the ratites (Palaeognathae), is used as an outgroup. The cladogram is based on the avian phylogenetic tree [10] using the ETE Toolkit [146].

Figure 4

Graphical dependence (according to [17,87]) of the integral indicator of genomic “variadicity” and specific chromosomal rearrangements (R₅; x-axis) on the total number of all rearrangements (y-axis) for eight Neognathae representatives: canary (A), blackbird (B), pigeon (P), houbara (H), woodcock (W), chicken (C), guineafowl (G) and duck (D).

Figure 5

Phylogenetic tree of birds (according to [9,150,151]). The chicken and turkey are located near the bottom of the tree, on the basal branch of Neognathae, and passerines (Passeri) are at the very top of the tree, on the evolutionarily youngest branch. Evolutionary distances between different taxa are presented conditionally.

Figure 6

Correlation between the success rate of probes (%; x-axis) and the evolutionary divergence of birds (million years ago; y-axis) resulting from cross-species DNA hybridization (according to [78,150]). Dark blue points and trend line, number of nodes on the phylogenetic tree; pink points and trend line, divergence time.