Novel Insights into Chromosome Evolution in Birds, Archosaurs, and Reptiles

Abstract

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 5 outgroup species using recently sequenced genomes across the avian family tree and a newly-developed algorithm. We identified EBRs and HSBs in ancestral bird, archosaurian (bird, crocodile, and dinosaur), and reptile chromosomes. Genes involved in the regulation of gene expression and biosynthetic processes were preferably located in HSBs, including for example, avian-specific HSBs enriched for genes involved in limb development. Within birds, some lineage-specific EBRs rearranged genes were related to distinct phenotypes, such as forebrain development in parrots. Our findings provide novel evolutionary insights into genome evolution in birds, particularly on how chromosome rearrangements likely contributed to the formation of novel phenotypes.

Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set

“…A total of 69 intrachromosomal EBRs were detected in the falcon lineage (Supplemental Table S8; Supplemental Results). Consistent with our previous report (Farré et al 2016), falcon intrachromosomal EBRs were found highly enriched for the LTR-ERV1 transposable elements (TEs; t-test P < 0.05) (Supplemental Table S9). Both fusion and fission EBRs were not significantly enriched for any type of TEs.…”

“…Regardless of the mechanism, comparisons of multiple animal genomes show that between EBRs are evolutionary stable homologous synteny blocks (HSBs). Our studies in mammals ) and birds (Farré et al 2016) suggest that at least the largest HSBs are maintained nonrandomly and are highly enriched for conserved noncoding elements (CNEs), many of which are gene regulatory sequences and miRNAs (Zhang et al 2014b). We recently hypothesized that a higher fraction of elements under negative selection involved in gene regulation and chromosome structure in avian genomes (∼7%) (Zhang et al 2014b) compared with mammals (∼4%) (Lindblad-Toh et al 2011) could contribute to some avian-specific phenotypes and the evolutionary stability of most avian karyotypes (Farré et al 2016).…”

“…There was no evidence of reciprocal translocations, and all microchromosomes remained intact, even when fused to larger chromosomes. Recently, we suggested possible mechanisms why avian genomes, with relatively rare exceptions, remain evolutionarily stable interchromosomally and why microchromosomes represent blocks of conserved synteny (Romanov et al 2014;Farré et al 2016). Absence of interchromosomal rearrangement (as seen in most birds) could suggest either an evolutionary advantage to retaining such a configuration or little opportunity for change.…”

“…We recently hypothesized that a higher fraction of elements under negative selection involved in gene regulation and chromosome structure in avian genomes (∼7%) (Zhang et al 2014b) compared with mammals (∼4%) (Lindblad-Toh et al 2011) could contribute to some avian-specific phenotypes and the evolutionary stability of most avian karyotypes (Farré et al 2016). While a high density of CNEs in avian multispecies (ms) HSBs supports this hypothesis (Farré et al 2016), a more definitive answer might be obtained by examining the fate of CNEs in the "interchromosomal EBRs" (flanking interchromosomal rearrangements) of an avian genome with a highly rearranged karyotype.…”

“…To identify CNE densities and the distribution associated with avian EBRs at the genome-wide level, we counted CNE bases in 1-kb windows overlapping EBRs and avian msHSBs >1.5 Mb (Farré et al 2016). The average density of CNEs in the EBR windows was lower (0.02) than in msHSBs (0.11).…”