Origin and evolution of avian microchromosomes

Abstract

The origin of avian microchromosomes has long been the subject of much speculation and debate. Microchromosomes are a universal characteristic of all avian species and many reptilian karyotypes. The typical avian karyotype contains about 40 pairs of chromosomes and usually 30 pairs of small to tiny microchromosomes. This characteristic karyotype probably evolved 100–250 million years ago. Once the microchromosomes were thought to be a non-essential component of the avian genome. Recent work has shown that even though these chromosomes represent only 25% of the genome; they encode 50% of the genes. Contrary to popular belief, microchromosomes are present in a wide range of vertebrate classes, spanning 400–450 million years of evolutionary history. In this paper, comparative gene mapping between the genomes of chicken, human, mouse and zebrafish, has been used to investigate the origin and evolution of avian microchromosomes during this period. This analysis reveals evidence for four ancient syntenies conserved in fish, birds and mammals for over 400 million years. More than half, if not all, microchromosomes may represent ancestral syntenies and at least ten avian microchromosomes are the product of chromosome fission. Birds have one of the smallest genomes of any terrestrial vertebrate. This is likely to be the product of an evolutionary process that minimizes the DNA content (mostly through the number of repeats) and maximizes the recombination rate of microchromosomes. Through this process the properties (GC content, DNA and repeat content, gene density and recombination rate) of microchromosomes and macrochromosomes have diverged to create distinct chromosome types. An ancestral genome for birds likely had a small genome, low in repeats and a karyotype with microchromosomes. A “Fission–Fusion Model” of microchromosome evolution based on chromosome rearrangement and minimization of repeat content is discussed.

Reassessment of genome size in turtle and crocodile based on chromosome measurement by flow karyotyping: close similarity to chicken

“…ACA has a few microchromosomes that are conserved between ACA and GGA, and that may have arisen in the reptile ancestor [11]. It is suggested that the formation of microchromosomes leads to a reduction of genome size [23]. We find that TSC and CNI genome sizes are closer to GGA than to ACA, and total GC content in GGA, TSC and CNI is higher than in ACA (figure 2b).…”

Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens)

“…This reasoning assumes that f is a precise estimate of selectable autozygosity. However, the simulation results suggest that individuals within an inbreeding class can vary widely in autozygosity even when the number of linkage groups is large, as is thought to be the case in birds (Thorneycroft, 1975;Burt, 2002). Therefore, some of the variation in fitness due to heterosis that is not accounted for by f may be reflected in H. If so, then SSR HFC's within inbreeding classes may be due to variation among identically inbred individuals in true autozygosity, rather than a result of local effects.…”

“…Although physical linkage groups in birds are likely to be small and numerous (Burt, 2002), bottlenecks and population structure can increase the level of linkage disequilibrium (Hansson and Westerberg, 2002), and perhaps falsely give the impression of local effects because each marker locus would represent a substantial portion of the genome. Thus, the general effects hypothesis can be rejected only after the variance in individual autozygosity for a known level of inbreeding has been accounted for (cf.…”

cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids

“…However, the karyotype of the common ancestor of extant sauropsids is thought to have contained both macrochromosomes and microchromosomes (Burt 2002;Norris et al 2004), although some lineages underwent frequent secondary fusion of microchromosomes resulting in no or few microchromosomes as seen in the reptilian family Crocodylidae and the avian family Falconiformes (Cohen & Gans 1970;De Boer & Sinoo 1984). In contrast, chromosome sizes are relatively uniform and there is no striking bias in inter-chromosomal GC-content in most mammals.…”

“…Although the evolutionary origin and intrinsic nature of this GC heterogeneity is not fully understood (Eyre-Walker & Hurst 2001), the existence of intra-genome GC Karyotypes of extant sauropsids (reptiles and birds) generally consist of two major components: macrochromosomes and microchromosomes (Burt 2002;Norris et al 2004). In chicken, cytogenetic observations indicate that microchromosomes exhibit a higher gene density (McQueen et al 1998;Smith et al 2000), a higher density of CpG islands (McQueen et al 1996) and a higher GC-content than macrochromosomes (Auer et al 1987;Andreozzi et al 2001).…”