Chromosome repatterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting

Abstract

Parrots (order: Psittaciformes) are the most common captive birds and have attracted human fascination since ancient times because of their remarkable intelligence and ability to imitate human speech. However, their genome organization, evolution and genomic relation with other birds are poorly understood. Chromosome painting with DNA probes derived from the flow-sorted macrochromosomes (1–10) of chicken (Gallus gallus, GGA) has been used to identify and distinguish the homoeologous chromosomal segments in three species of parrots, i.e., Agapornis roseicollis (peach-faced lovebird); Nymphicus hollandicus (cockatiel) and Melopsittacus undulatus (budgerigar). The ten GGA macrochromosome paints unequivocally recognize 14 to 16 hybridizing regions delineating the conserved chromosomal segments for the respective chicken macrochromosomes in these representative parrot species. The cross-species chromosome painting results show that, unlike in many other avian karyotypes with high homology to chicken chromosomes, dramatic rearrangements of the macrochromosomes have occurred in parrot lineages. Among the larger GGA macrochromosomes (1–5), chromosomes 1 and 4 are conserved on two chromosomes in all three species. However, the hybridization pattern for GGA 4 in A. roseicollis and M. undulatus is in sharp contrast to the most common pattern known from hybridization of chicken macrochromosome 4 in other avian karyotypes. With the exception of A. roseicollis, chicken chromosomes 2, 3 and 5 hybridized either completely or partially to a single chromosome. In contrast, the smaller GGA macrochromosomes 6, 7 and 8 displayed a complex hybridization pattern: two or three of these macrochromosomes were found to be contiguously arranged on a single chromosome in all three parrot species. Overall, the study shows that translocations and fusions in conjunction with intragenomic rearrangements have played a major role in the karyotype evolution of parrots. Our inter-species chromosome painting results unequivocally illustrate the dynamic reshuffling of ancestral chromosomes among the karyotypes ofPsittaciformes.

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

“…Larkin et al (2009) suggested that homologous synteny blocks and evolutionary breakpoint regions are subject to different evolutionary pressures. As further avian genomes are published, especially those with atypical karyotypes (for example, Falconiformes and Psittaciformes (de Oliveira et al, 2005(de Oliveira et al, , 2010Nanda et al, 2007;Nishida et al, 2008;Nie et al, 2009), we will be able to test the hypothesis that blocks of ordered genes have been preserved through evolution, and that these are reflected in the syntenic blocks seen here. Further species that have been of interest in zoo-FISH studies and would thus be likely candidates for studies in addition to the Falconiformes and Psittaciformes mentioned above include other Galliformes (Shibusawa et al, 2004a, b) and a range of species from orders such as Anseriformes and Passeriformes (Guttenbach et al, 2003).…”

Chromosomal Evolution in Psittaciformes. Revisited

“…Agapornis roseicollis karyotype has the lowest diploid number found in Psittaciformes, and an unusual high number of macrochromosomes (ten autosome pairs), suggesting that several fusion events have conformed this karyogram (Nanda et al, 2007). It is difficult to propose karyological relationships between this species and other parrots.…”

“…Present day availability of some avian genome sequences, or techniques based on chromosome painting with DNA probes have improved our ability to reconstruct chromosome evolutionary changes (de Oliveira Furo et al, 2015;Nanda, Karl, Griffin, Schartl, & Schmid, 2007;Seibold-Torres et al, 2016). 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).…”

“…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). 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).…”

“…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).…”