Chromosome-level assembly reveals extensive rearrangement in saker falcon and budgerigar, but not ostrich, genomes

Abstract

BackgroundThe number of de novo genome sequence assemblies is increasing exponentially; however, relatively few contain one scaffold/contig per chromosome. Such assemblies are essential for studies of genotype-to-phenotype association, gross genomic evolution, and speciation. Inter-species differences can arise from chromosomal changes fixed during evolution, and we previously hypothesized that a higher fraction of elements under negative selection contributed to avian-specific phenotypes and avian genome organization stability. The objective of this study is to generate chromosome-level assemblies of three avian species (saker falcon, budgerigar, and ostrich) previously reported as karyotypically rearranged compared to most birds. We also test the hypothesis that the density of conserved non-coding elements is associated with the positions of evolutionary breakpoint regions.ResultsWe used reference-assisted chromosome assembly, PCR, and lab-based molecular approaches, to generate chromosome-level assemblies of the three species. We mapped inter- and intrachromosomal changes from the avian ancestor, finding no interchromosomal rearrangements in the ostrich genome, despite it being previously described as chromosomally rearranged. We found that the average density of conserved non-coding elements in evolutionary breakpoint regions is significantly reduced. Fission evolutionary breakpoint regions have the lowest conserved non-coding element density, and intrachromomosomal evolutionary breakpoint regions have the highest.ConclusionsThe tools used here can generate inexpensive, efficient chromosome-level assemblies, with > 80% assigned to chromosomes, which is comparable to genomes assembled using high-density physical or genetic mapping. Moreover, conserved non-coding elements are important factors in defining where rearrangements, especially interchromosomal, are fixed during evolution without deleterious effects.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1550-x) contains supplementary material, which is available to authorized users.

Genome of an iconic Australian bird: High‐quality assembly and linkage map of the superb fairy‐wren (Malurus cyaneus)

“…The chromosomes were reordered in the circos plot to match the homologous chromosomes of the M. cyaneus genome for comparison. The Falco peregrinus genome, like other falconid genomes, has consistently been shown to have many rearrangements (Nishida et al, ; O’Connor et al, ). Interestingly the other raptor genome, Aquila chrysaetos , also exhibits high levels of rearrangements despite being distantly related and converging on raptorial lifestyles.…”

“…Synteny of the macrochromosomes is largely conserved between the fairy-wren and other bird genome assemblies (Figure 4) (Nishida et al, 2008;O'Connor et al, 2018). Interestingly the other raptor genome, Aquila chrysaetos, also exhibits high levels of rearrangements despite being distantly related and converging on raptorial lifestyles.…”

New genome assembly of the barn owl (Tyto alba alba)

“…In addition, the barn owl genome appears to have few rearrangements or miss‐assemblies when compared to the zebra finch genome. High chromosome synteny is observed in most birds, except in the Falconiformes and the Psittaciformes containing high levels of interchromosomal rearrangements (O'Connor et al, ).…”

“…In addition, the barn owl genome appears to have few rearrangements or miss-assemblies when compared to the zebra finch genome. High chromosome synteny is observed in most birds, except in the Falconiformes and the Psittaciformes containing high levels of interchromosomal rearrangements(O'Connor et al, 2018).The GC content impacts the short-read sequencing, as has been shown previously (see for example Botero-Castro et al,Figure 5b,(Botero-Castro et al, 2017). Fifteen percent of genes present in most vertebrate lineages and thought to be missing in the avian genomes(Lovell et al, 2014) are located in very GC-rich mini-chromosomes(Bornelov et al, 2017;Botero-Castro et al, 2017).…”

Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

“…The evolution of associated traits of flight loss and gigantism has facilitated ratites' adaption for cursoriality, and had profound impacts on their genome evolution. Compared to the genomes of other smaller and volant birds, the ostrich genome is characterized with much lower rates of substitutions 9 and insertions/deletions, transposon removal 10 , and very few intrachromosomal rearrangements even when being compared with the distantly-related chicken 11 . This parallels the similar comparisons between elephants or whales vs. other mammals 10,[12][13][14] , and can be explained by the fact that species with a larger body size tend to have a longer generation time and a lower metabolic rate, hence a reduced mutation rate 12,15 .…”