Avian cytogenetics goes functional

Whole chromosomes (and sub-chromosomal homologous synteny blocks (HSBs)) have great significance in molecular studies of genome evolution. In birds, our ability to define chromosomes and HSBs precisely has however been impeded by a near intractable karyotype and so has focused primarily on comparative molecular cytogenetics (zoo-FISH) of the largest chromosomes (1–10+Z). Availability of multiple avian genome sequence assemblies has however allowed us, for the first time, to identify chromosomal syntenies across species. In recent work we have made use of comparative maps for 20+ avian genome assemblies (plus out-groups) and presented them on “Evolution Highway” an open-access, interactive freely available comparative chromosome browser designed to store and visualise comparative chromosome maps. This browser (http://evolutionhighway.ncsa.uiuc.edu) is used to visualize comparative genome organization and to identify and visualize the different types of evolutionary breakpoint regions (EBRs) in chromosomes, e.g., lineage specific, ordinal, superordinal, and reuse. Comparative analysis of all available genomes is providing insight into the mechanisms of chromosome change through correlation of EBRs with transposable elements and non-allelic homologous recombination. Gene ontology analysis is revealing interesting correlations with avian specific phenotype and function. Focus on six genomes (chicken, turkey, duck, zebra finch, ostrich and budgerigar) with both the largest N50s and supporting molecular cytogenetic information, has allowed us to assemble a putative ancestral avian karyotype and identify the key changes that led to the gross genome organization of representatives in the major avian clades (Palaeognathae, Galliformes, Anseriformes and Neoaves). We describe, for the first time, numerous inter-chromosomal rearrangements in a Paleoganthaeous bird (the ostrich), plus rearrangements in the budgerigar (Psattaciformes) and 15 other species. Intra-chromosomal evolutionary change in all species studied, can be derived, most parsimoniously, by a series of inversions, inter-chromosomal rearrangements by fissions and fusions. Increased chromosome rearrangement is associated with differentiation in certain clades, with the most intrachromosomal changes (primarily inversions) occurring in the zebra finch (Passeriformes) since its divergence from its sister group, the Psittaciformes 54MYA, This is coincident with the evolution of passerine-specific phenotypes e.g. vocal learning. Results also suggest that the Galloanserae (especially chicken) underwent the fewest changes compared to the ancestral karyotype; notably these birds appear, from fossil evidence, to be the most similar to ancient avian ancestors. We thus present the most comprehensive analysis of chromosomal rearrangements in birds to date and draw novel conclusions about their mechanisms of origin and association with avian-specific phenotypic features.