The evolution of the avian genome as revealed by comparative molecular cytogenetics

Abstract

Birds are characterised by feathers, flight, a small genome and a very distinctive karyotype. Despite the large numbers of chromosomes, the diploid count of 2n ≈ 80 has remained remarkably constant with 63% of birds where 2n = 74–86, 24% with 2n = 66–74 and extremes of 2n = 40 and 2n = 142. Of these, the most studied is the chicken (2n = 78), and molecular cytogenetic probes generated from this species have been used to further understand the evolution of the avian genome. The ancestral karyotype is, it appears, very similar to that of the chicken, with chicken chromosomes 1, 2, 3, 4q, 5, 6, 7, 8, 9, 4p and Z representing the ancestral avian chromosomes 1–10 + Z; chromosome 4 being the most ancient. Avian evolution occurred primarily in three stages: the divergence of the group represented by extant ratites (emu, ostrich etc.) from the rest; divergence of the Galloanserae (chicken, turkey, duck, goose etc.) – the most studied group; and divergence of the ‘land’ and ‘water’ higher birds. Other than sex chromosome differentiation in the first divergence there are no specific changes associated with any of these evolutionary milestones although certain families and orders have undergone multiple fusions (and some fissions), which has reduced their chromosome number; the Falconiformes are the best described. Most changes, overall, seem to involve chromosomes 1, 2, 4, 10 and Z where the Z changes are intrachromosomal; there are also some recurring (convergent) events. Of these, the most puzzling involves chromosomes 4 and 10, which appear to have undergone multiple fissions and/or fusions throughout evolution – three possible hypotheses are presented to explain the findings. We conclude by speculating as to the reasons for the strange behaviour of these chromosomes as well as the role of telomeres and nuclear organisation in avian evolution.

The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds

“…The short arm of GGA4 is GC-rich, preserving the feature of GC-rich bird microchromosome (McQueen et al 1996(McQueen et al , 1998 Griffin et al 2007). We previously delineated the process of karyotypic evolution of the Galliformes by comparing the chromosome painting data of 13 Galliformes species with their molecular phylogenetic tree constructed with the mitochondrial DNA sequences, and consequently proposed that the karyotype of emu is identical with the ancestral karyotype of the Galliformes (at least for the largest chromosome pairs) (Shibusawa et al 2004b).…”

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

“…This could pose a problem if chromosomal rearrangements have been frequent and differentiated the chicken and zebra finch karyotypes. However, the rates of translocation, fusion, and fission have generally been low during avian genome evolution (Burt et al 1999;Bourque et al 2005), and, on the whole (see Supplemental Material), chicken and zebra finch chromosomes 1-10 are syntenic (Griffin et al 2007). As the Z chromosome is similar in size to autosomes 5 and 6 in chicken, and to obtain a reasonably large set of genes for comparison, we extracted data from genes located on chicken chromosomes 1-10.…”

Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints

“…Avian karyotypes are also characteristic with nearly two-thirds of birds having a diploid chromosome number of around 80 and the vast majority having a large number of microchromosomes (Christidis, 1990). Between 2004 and 2010 the chicken genome was the only avian representative being completely characterized and karyotyped (Hillier et al, 2004;Masabanda et al, 2004), but this nevertheless has allowed cross-species chromosome painting to numerous other birds (reviewed in Griffin et al, 2007) and BAC mapping to build physical maps of a few others. These include turkey, duck and zebra finch Skinner et al, 2009a;Volker et al, 2010).…”