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

Romanov MN, Farré M, Lithgow PE, Fowler KE, Skinner BM, O'Connor R, Fonseka G, Backström N, Matsuda Y, Nishida C, Houde P, Jarvis ED, Ellegren H, Burt DW, Larkin DM, Griffin DK - BMC Genomics (2014)

Bottom Line: Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace.All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count.Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, University of Kent, Canterbury CT2 7NJ, UK. dlarkin@rvc.ac.uk.

ABSTRACT

Background: The 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.

Results: Focusing 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.

Conclusions: Results 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.

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Number of interchromosomal rearrangements involving microchromosomes. Plotted against deviation from n = 40 for each species in which chromosome number is published (Table 3). Analysis suggests that haploid chromosome number effectively is a reflection of number of microchromosomal rearrangement, except in ostrich (red dot). Best-fit line is drawn excluding ostrich outlier (R2 = 0.7, P = 0.0002 if ostrich is excluded; R2 = 0.3, P = 0.03 if ostrich is included).
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Fig6: Number of interchromosomal rearrangements involving microchromosomes. Plotted against deviation from n = 40 for each species in which chromosome number is published (Table 3). Analysis suggests that haploid chromosome number effectively is a reflection of number of microchromosomal rearrangement, except in ostrich (red dot). Best-fit line is drawn excluding ostrich outlier (R2 = 0.7, P = 0.0002 if ostrich is excluded; R2 = 0.3, P = 0.03 if ostrich is included).

Mentions: For chicken, turkey, zebra finch and duck, inter-macrochromosomal changes have been previously described, i.e. chromosome 4 fusion for chicken, chromosome 2 fission for turkey, chromosome 1 fission for zebra finch, and no changes in duck [12–14] in these four species. In the current analyses, however, results suggested that there were at least 26 interchromosomal differences between chicken and ostrich, and 40 between chicken and budgerigar for all chromosomes (Table 2), with the changes in the budgerigar lineage occurring since the passeriform-psittaciform divergence (~54 MYA). Considering microchromosomes alone and using data pertaining to numbers of interchromosomal rearrangements for the remaining 15 species [37], results suggested that microchromosomal rearrangement was rare, except where the species of interest had been previously known to have an unusually large or small number of chromosomes (Table 3). In other words, as illustrated in Figure 6, there was a statistically significant correlation (R2 = 0.3; P = 0.03) between number of interchromosomal rearrangements and published deviation from a haploid chromosome number of 40. The exception to this “rule” was the ostrich (2n = 80), with 26 interchromosomal differences, 11 involving the microchromosomes, results suggesting significant rearrangement while maintaining the overall karyotypic structure. Indeed, if ostrich is excluded from the analysis outlined in Table 3 and Figure 6, the statistical significance of the association increases markedly (R2 = 0.7, P = 0.0002).Table 3


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

Romanov MN, Farré M, Lithgow PE, Fowler KE, Skinner BM, O'Connor R, Fonseka G, Backström N, Matsuda Y, Nishida C, Houde P, Jarvis ED, Ellegren H, Burt DW, Larkin DM, Griffin DK - BMC Genomics (2014)

Number of interchromosomal rearrangements involving microchromosomes. Plotted against deviation from n = 40 for each species in which chromosome number is published (Table 3). Analysis suggests that haploid chromosome number effectively is a reflection of number of microchromosomal rearrangement, except in ostrich (red dot). Best-fit line is drawn excluding ostrich outlier (R2 = 0.7, P = 0.0002 if ostrich is excluded; R2 = 0.3, P = 0.03 if ostrich is included).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4362836&req=5

Fig6: Number of interchromosomal rearrangements involving microchromosomes. Plotted against deviation from n = 40 for each species in which chromosome number is published (Table 3). Analysis suggests that haploid chromosome number effectively is a reflection of number of microchromosomal rearrangement, except in ostrich (red dot). Best-fit line is drawn excluding ostrich outlier (R2 = 0.7, P = 0.0002 if ostrich is excluded; R2 = 0.3, P = 0.03 if ostrich is included).
Mentions: For chicken, turkey, zebra finch and duck, inter-macrochromosomal changes have been previously described, i.e. chromosome 4 fusion for chicken, chromosome 2 fission for turkey, chromosome 1 fission for zebra finch, and no changes in duck [12–14] in these four species. In the current analyses, however, results suggested that there were at least 26 interchromosomal differences between chicken and ostrich, and 40 between chicken and budgerigar for all chromosomes (Table 2), with the changes in the budgerigar lineage occurring since the passeriform-psittaciform divergence (~54 MYA). Considering microchromosomes alone and using data pertaining to numbers of interchromosomal rearrangements for the remaining 15 species [37], results suggested that microchromosomal rearrangement was rare, except where the species of interest had been previously known to have an unusually large or small number of chromosomes (Table 3). In other words, as illustrated in Figure 6, there was a statistically significant correlation (R2 = 0.3; P = 0.03) between number of interchromosomal rearrangements and published deviation from a haploid chromosome number of 40. The exception to this “rule” was the ostrich (2n = 80), with 26 interchromosomal differences, 11 involving the microchromosomes, results suggesting significant rearrangement while maintaining the overall karyotypic structure. Indeed, if ostrich is excluded from the analysis outlined in Table 3 and Figure 6, the statistical significance of the association increases markedly (R2 = 0.7, P = 0.0002).Table 3

Bottom Line: Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace.All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count.Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, University of Kent, Canterbury CT2 7NJ, UK. dlarkin@rvc.ac.uk.

ABSTRACT

Background: The 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.

Results: Focusing 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.

Conclusions: Results 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.

Show MeSH
Related in: MedlinePlus