Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor

Abstract

BackgroundThe availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative molecular cytogenetics of only the largest chromosomes. Here, novel whole genome sequence information from 21 avian genome sequences (most newly assembled) made available on an interactive browser (Evolution Highway) was analyzed.ResultsFocusing on the six best-assembled genomes allowed us to assemble a putative karyotype of the dinosaur ancestor for each chromosome. Reconstructing evolutionary events that led to each species’ genome organization, we determined that the fastest rate of change occurred in the zebra finch and budgerigar, consistent with rapid speciation events in the Passeriformes and Psittaciformes. Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace. Analyzing chicken and zebra finch, we found little evidence to support the hypothesis of an association of evolutionary breakpoint regions with recombination hotspots but some evidence to support the hypothesis that microchromosomes largely represent conserved blocks of synteny in the majority of the 21 species analyzed. All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count. Ostrich, however, appeared to retain an overall karyotype structure of 2n = 80 despite undergoing a large number (26) of hitherto un-described interchromosomal changes.ConclusionsResults suggest that mechanisms exist to preserve a static overall avian karyotype/genomic structure, including the microchromosomes, with widespread interchromosomal change occurring rarely (e.g., in ostrich and budgerigar lineages). Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1060) contains supplementary material, which is available to authorized users.

Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set

“…This might also explain why falcon-specific fission breakpoints appear to be reused in other avian lineages as intrachromosomal EBRs. The study of intrachromosomal changes in pigeons, falcons (this study), and Passeriform species (Skinner and Griffin 2012;Romanov et al 2014) suggests that these events might have a less dramatic effect on cis gene regulation than interchromosomal events. Indeed, intrachromosomal EBRs appear in regions of significantly higher CNE density than interchromosomal EBRs.…”

“…There was no evidence of reciprocal translocations, and all microchromosomes remained intact, even when fused to larger chromosomes. Recently, we suggested possible mechanisms why avian genomes, with relatively rare exceptions, remain evolutionarily stable interchromosomally and why microchromosomes represent blocks of conserved synteny (Romanov et al 2014;Farré et al 2016). Absence of interchromosomal rearrangement (as seen in most birds) could suggest either an evolutionary advantage to retaining such a configuration or little opportunity for change.…”

Avian genomics: fledging into the wild!

“…Interestingly, it seems that the chicken lineage most closely resembles the dinosaur avian ancestor (Romanov et al 2014). Looking deeper at specific genes of the avian genomes revealed several patterns of adaptation and further connections between ecology, biology, and genetics.…”

Chromosomal Evolution in Psittaciformes. Revisited

“…Despite interchromosome conservation, intrachromosome changes are considered common (Nanda et al, 2007;Skinner & Griffin, 2012). A correlation between rates of speciation, and the observed number of intrachromosome rearrangements has been suggested, as a faster rate of change has been observed in the most diverging orders Passeriformes and Psittaciformes (de Oliveira Furo et al, 2015;Nanda et al, 2007;Romanov et al, 2014;Seibold-Torres et al, 2016;Skinner & Griffin, 2012). It has also been suggested that the presence of syntenic blocks of genome, associated with evolutionary breakpoint hotspot regions, may explain most events in the avian chromosomal evolution (Larkin et al, 2009;Skinner & Griffin, 2012).…”

“…Interchromosome evolutionary changes have been considered to occur rarely during avian diversification suggesting that mechanisms exist to preserve a static overall karyotype structure (Romanov et al, 2014). Despite interchromosome conservation, intrachromosome changes are considered common (Nanda et al, 2007;Skinner & Griffin, 2012).…”