Remarkably high repeat content in the genomes of sparrows: the importance of genome assembly completeness for transposable element discovery

Abstract

ABSTRACTTransposable elements (TE) play critical roles in shaping genome evolution. However, the highly repetitive sequence content of TEs is a major source of assembly gaps. This makes it difficult to decipher the impact of these elements on the dynamics of genome evolution. The increased capacity of long-read sequencing technologies to span highly repetitive regions of the genome should provide novel insights into patterns of TE diversity. Here we report the generation of highly contiguous reference genomes using PacBio long read and Omni-C technologies for three species of sparrows in the family Passerellidae. To assess the influence of sequencing technology on TE annotation, we compared these assemblies to three chromosome-level sparrow assemblies recently generated by the Vertebrate Genomes Project and nine other sparrow species generated using a variety of short- and long-read technologies. All long-read based assemblies were longer in length (range: 1.12-1.41 Gb) than short-read assemblies (0.91-1.08 Gb). Assembly length was strongly correlated with the amount of repeat content, with longer genomes showing much higher levels of repeat content than typically reported for the avian order Passeriformes. Repeat content for the Bell’s sparrow (31.2% of genome) was the highest level reported to date for a songbird genome assembly and was more in line with woodpecker (order Piciformes) genomes. CR1 LINE elements retained from an expansion that occurred 25-30 million years ago were the most abundant TEs in the song sparrow genome. Although the other five sparrow species also exhibit evidence for a spike in CR1 LINE activity at 25-30 million years ago, LTR elements stemming from more recent expansions were the most abundant elements in these species. LTRs were uniquely abundant in the Bell’s sparrow genome deriving from two recent peaks of activity. Higher levels of repeat content (79.2-93.7%) were found on the W chromosome relative to the Z (20.7-26.5) or autosomes (16.1-30.9%). These patterns support a dynamic model of transposable element expansion and contraction underpinning the seemingly constrained and small sized genomes of birds. Our work highlights how the resolution of difficult-to-assemble regions of the genome with new sequencing technologies promises to transform our understanding of avian genome evolution.