Migrators within migrators: exploring transposable element dynamics in the monarch butterfly, Danaus plexippus

Abstract

Background: Lepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly is available for the monarch butterfly (Danaus plexippus), but it lacks an in-depth transposable element (TE) annotation, presenting an opportunity to explore monarch TE dynamics and the impact of TEs on shaping the monarch genome.

Results: We find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1-2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes.

Conclusions: We provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.

Keywords: Butterfly; Danaus plexippus; Genome Evolution; Genomic Deletion; Lepidoptera; Repeat; TE Annotation; Transposon.

Fig. 1

TE content in the monarch, D. chrysippus and D. melanippus. Major TE types are represented by different colours indicated in the key (A) Pie charts illustrating proportions of each Danaus genome comprised of the main TE classifications. (B) Repeat landscapes for each Danaus species. The x axis indicates the level of Kimura 2-parameter genetic distance observed between TE insertions and their respective consensus sequences in percent. More recent elements are located to the right of the x axis. The y axis indicates the percentage of the genome occupied by TE insertions of each genetic distance class

Fig. 2

Processes leading to genome size differences between the monarch, D. chrysippus, and D. melanippus. (A) Three hypotheses leading to observed differences in genome size between Danaus species. Hypotheses indicated by colours in the key. (B) Shared and unique TE families across the three Danaus species. Numbers indicate distinct TE families. Percentages indicate proportion of total TE families found in each section of the Venn diagram. (C) TE coverage in each Danaus species split by TE shared status. Major TE types are represented by different colours indicated in the key

Fig. 3

TE location in different genomic compartments in the monarch. Major TE types are represented by different colours indicated in the key. (A) Quantity of TE base pairs found in different genomic compartments. (B) Proportion of each genomic compartment contributed by TEs

Fig. 4

Violin plot showing kilobases of TE sequence per 100 kb window across the genome for each of the main TE classifications. Red points show the mean kilobases of TE sequence per 100 kb

Fig. 5

Karyoplots illustrating monarch chromosomes. Grey boxes represent chromosomes, with black regions representing genic regions of each chromosome. (A) Above each chromosome, TE density is shown for 100 kb windows, with major TE types represented by different colours indicated in the key. (B) Above each chromosome, TE hotspots and coldspots are shown, with severity represented by the different colours indicated in the key

Fig. 6

Violin plot illustrating the estimated insertion time (Mya) for each of the major TE types, represented by different colours indicated in the key. The black bar shows the estimated divergence time of the monarch, approximately 32Mya [66]

Fig. 7

TE age against copy number. Major TE types are represented by different colours indicated in the key. X axis shows estimated age of each TE family, Y axis shows log10 transformed TE copy number identified in the monarch