Genome Rearrangements Contribute to Vocal Learning in Birds: A Model to Study Evolution of Speech?

Homologous synteny blocks (HSBs) and evolutionary breakpoint regions (EBRs) in mammalian chromosomes are enriched for distinct DNA features, contributing to distinct phenotypes. To reveal HSB and EBR roles in avian evolution, we performed a sequence-based comparison of 21 avian and five outgroup species using recently sequenced genomes across the avian family tree. We identified EBRs and HSBs in ancestral bird, archosaurian (bird, crocodile, dinosaur), and reptile chromosomes. Archosaurian-specific HSBs were enriched for genes that function in retina structures, while avian-specific HSBs for genes involved in limb development. The average rate of rearrangements in birds is ~1.25 EBRs per million years; however, bursts of genomic reorganization occurred in several avian lineages. For example, the origin of Neognathae was accompanied by an elevated rate of chromosome rearrangements. Intriguingly, all vocal-learning species had significantly higher rates of rearrangements than those of close vocal nonlearning relatives  and even higher relative to all vocal nonlearning species. EBRs leading to budgerigar after the divergence from the Passerimorphae ancestor tended to reshuffle genes involved in forebrain development. Remarkably, the forebrain development GO term was enriched in avian and archousaurian msHSBs as well. However, the gene pathways affected by EBRs and msHSBs were different. This example indicates that both EBRs and msHSBs are sources of variation used by natural selection to form complex phenotypes over evolutionary time. Our findings provide novel evolutionary insights into genome evolution in birds, particularly how chromosome rearrangements contributed to formation of phenotypes that make vocal-learning birds excellent models to study evolution of speech.