Millipede genomes reveal unique adaptations during myriapod evolution

Abstract

The Myriapoda, composed of millipedes and centipedes, is a fascinating but poorly understood branch of life, including species with a highly unusual body plan and a range of unique adaptations to their environment. Here, we sequenced and assembled 2 chromosomal-level genomes of the millipedes Helicorthomorpha holstii (assembly size = 182 Mb; shortest scaffold/contig length needed to cover 50% of the genome [N50] = 18.11 Mb mainly on 8 pseudomolecules) and Trigoniulus corallinus (assembly size = 449 Mb, N50 = 26.78 Mb mainly on 17 pseudomolecules). Unique genomic features, patterns of gene regulation, and defence systems in millipedes, not observed in other arthropods, are revealed. Both repeat content and intron size are major contributors to the observed differences in millipede genome size. Tight Hox and the first loose ecdysozoan ParaHox homeobox clusters are identified, and a myriapod-specific genomic rearrangement including Hox3 is also observed. The Argonaute (AGO) proteins for loading small RNAs are duplicated in both millipedes, but unlike in insects, an AGO duplicate has become a pseudogene. Evidence of post-transcriptional modification in small RNAs-including species-specific microRNA arm switching-providing differential gene regulation is also obtained. Millipedes possesses a unique ozadene defensive gland unlike the venomous forcipules found in centipedes. We identify sets of genes associated with the ozadene that play roles in chemical defence as well as antimicrobial activity. Macrosynteny analyses revealed highly conserved genomic blocks between the 2 millipedes and deuterostomes. Collectively, our analyses of millipede genomes reveal that a series of unique adaptations have occurred in this major lineage of arthropod diversity. The 2 highquality millipede genomes provided here shed new light on the conserved and lineagespecific features of millipedes and centipedes. These findings demonstrate the importance of the consideration of both centipede and millipede genomes-and in particular the reconstruction of the myriapod ancestral situation-for future research to improve understanding of arthropod evolution, and animal evolutionary genomics more widely.

Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci, but consistently depends on chromosome size

“…As recently reported in millipedes (31), genomes with more repetitive elements show significant expansions in intron size. We explored this effect in Heliconius by looking at the composition of annotated gene models in SFCs.…”

“…We further found that, within species, intron length for genes on SFCs are significantly longer than for LFCs or NFCs (Wilcoxon rank-sum test 'greater'; P ≤ 2.63x10 -14 ) ( Figure S15). This pattern is highly similar to that of repeat content suggesting a correlation between the two (31). Indeed, SFC introns contain significantly higher amounts of transposable elements than would be predicted by their length (P ≤ 6.7x10 -09 ; elevation for intergenic regions 0.79±0.03; elevation for intronic regions 0.67±0.02).…”

Chromosome-level reference genome of the European wasp spider Argiope bruennichi: a resource for studies on range expansion and evolutionary adaptation

“…We obtained repeat content estimates, for which the repeats were masked using RepeatModeler and RepeatMasker, for 3 insect species ( Bombus terrestris, Drosophila melanogaster , and Rhodnius prolixus [ 73 ]) and 7 tick and mite species ( Ixodes persulcatus, Haemaphysalis longicornis, Dermacentor silvarum, Hyalomma asiaticum, Rhipicephalus sanguineus,Rhipicephalus microplus , and Ixodes scapularus [ 74 ]). We additionally downloaded the genomes of 4 more arthropod species, generated custom species-specific repeat libraries with RepeatModeler, and masked the genomes with RepeatMasker to avoid any issues of under- or overmasking using other repeat-masking programs: a butterfly, Heliconius melpomene [ 75 ]; a beetle, Tribolium castaneum [ 76 ]; a millipede, Helicorthomorpha holstii [ 77 ]; and a scorpion, Centruroides sculpturatus [ 7 , 33 ]. The percentage of total repetitive content for all of these species is presented in Table 4 .…”

Sea anemone genomes reveal ancestral metazoan chromosomal macrosynteny

“…5a). Among protostomes, we observed that the lophotrochozoan Ram's horn worm Streplosbio benedicti 39 and the sea scallop Patinopecten yessoensis 3 , as well as the ecdysozoan millipede Trigoniulus corallinus 40 , retained many macrosyntenic links (Fig. 5a).…”