Bursts of recent transposable element activity and signatures of element removal in the monarch genome, Danaus plexippus

Background: Lepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly of the monarch butterfly (Danaus plexippus), famous for its North American migration, is available but lacks an in-depth transposable element (TE) annotation. This provides an opportunity to explore host-TE interactions, and the impact TEs have in shaping the monarch genome. Results: 6.47% of the monarch genome is comprised of TEs, a reduction of 6.59% compared to the original TE annotation performed on the draft genome assembly. TE content is low compared to two closely related species, Danaus chrysippus (26.70%) and Danaus melanippus (11.87%). The biggest contributors to genome size in the monarch are LINEs and Penelope-like elements, and 37.7% of TE content is contributed by five newly identified TE families (two LINE, two Penelope-like, and one SINE). Some young DNA TE families show similar activity profiles to these LINEs, with their success putatively due to horizontal transposon transfer from species sharing the same environment. There are several recent peaks of TE activity in the monarch, with little evidence for peaks of activity more anciently. LINE fragments demonstrate signatures of genomic deletions as reported by studies on Heliconius butterflies, indicating a high rate of TE turnover. Given previous associations in other species, we investigated the association of TEs with wing colouration and immune genes. We find a single unclassified element 7kb upstream of the myosin gene locus, associated with wing colouration, and 49 immune genes with TEs within 5kb upstream of the transcription start site, presenting the potential for the involvement of TEs in regulatory functions. Conclusions: We provide an in-depth TE annotation and analysis of TE diversity and evolution for the monarch genome. We identify highly successful novel DNA TE families, mirroring the activity profile of the most successful LINEs. We also find evidence of ongoing TE expansion and removal in the monarch, highlighting the dynamic nature of repeat content in genomes over time. Further in-depth comparative studies across closely related species will be beneficial to our understanding of the evolutionary dynamics of TEs and the processes leading to their contrasting distributions.