Comparison of the Chinese bamboo partridge and red Junglefowl genome sequences highlights the importance of demography in genome evolution

G. P. Tiley, R. T. Kimball, E. L. Braun, J. G. Burleigh

Recent large-scale whole genome sequencing efforts in birds have elucidated broad patterns of avian phylogeny and genome evolution. However, despite the great interest in economically important phasianids like Gallus gallus (Red Junglefowl, the progenitor of the chicken), we know little about the genomes of closely related species. Gallus gallus is highly sexually dichromatic and polygynous, but its sister genus, Bambusicola, is smaller, sexually monomorphic, and monogamous with biparental care. We sequenced the genome of Bambusicola thoracicus (Chinese Bamboo Partridge) using a single insert library to test hypotheses about genome evolution in galliforms. Selection acting at the phenotypic level could result in more evidence of positive selection in the Gallus genome than in Bambusicola. However, the historical range size of Bambusicola was likely smaller than Gallus, and demographic effects could lead to higher rates of nonsynonymous substitution in Bambusicola than in Gallus. We generated a genome assembly suitable for evolutionary analyses. We examined the impact of selection on coding regions by examining shifts in the average nonsynonymous to synonymous rate ratio (dN/dS) and the proportion of sites subject to episodic positive selection. We observed elevated dN/dS in Bambusicola relative to Gallus, which is consistent with our hypothesis that demographic effects may be important drivers of genome evolution in Bambusicola. We also demonstrated that alignment error can greatly inflate estimates of the number of genes that experienced episodic positive selection and heterogeneity in dN/dS. However, overall patterns of molecular evolution were robust to alignment uncertainty. Bambusicola thoracicus has higher estimates of heterozygosity than Gallus gallus, possibly due to migration events over the past 100,000 years. Our results emphasized the importance of demographic processes in generating the patterns of variation between Bambusicola and Gallus. We also demonstrated that genome assemblies generated using a single library can provide valuable insights into avian evolutionary history and found that it is important to account for alignment uncertainty in evolutionary inferences from draft genomes.