Comparative genomics reveals the dynamics of chromosome evolution in Lepidoptera

nature ecology & evolution Article https://doi.org/10.1038/s41559-024-02329-4 Comparative genomics reveals the dynamics of chromosome evolution in Lepidoptera Received: 9 October 2023 Accepted: 12 January 2024 Published online: xx xx xxxx Check for updates Charlotte J. Wright 1 , Lewis Stevens Mara Lawniczak 1 & Mark Blaxter 1 several times across the tree of life, including in nematodes, four times in plants and multiple times in arthropods13–18. The most speciose of these holocentric groups is Amphiesmenoptera, comprising the insect orders Lepidoptera (moths and butterflies) and Trichoptera (caddisflies), which together account for 15% of all described eukaryotic species19,20. The convergent evolution of holocentricity in many speciose groups indicates that this alternative solution to accurate segregation of chromosomes may be evolutionarily advantageous. Holocentric chromosomes are suggested to facilitate rapid karyotypic evolution as fragments derived from fission could maintain kinetochore function21,22. Lepidoptera are the most karyotypically diverse group of any non-polyploid eukaryote, with haploid chromosome numbers (hereafter chromosome number, n) ranging from 5 to 223 (refs. 23,24). However, most species have haploid counts of n = 29–31 (refs. 25,26), indicating that further mechanisms must constrain holocentric karyotype evolution. Indeed, chromosome numbers and their gene contents are generally stable over evolutionary time in both holocentric and monocentric taxa27. Changes in chromosome number alter the recombination rate28,29. In Lepidoptera, where recombination only occurs in males (ZZ), there Tree of Life, Wellcome Sanger Institute, Cambridge, UK. 2Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, UK. e-mail: ; Nature Ecology & Evolution , 2 Chromosomes are a central unit of genome organization. One-tenth of all described species on Earth are butterflies and moths, the Lepidoptera, which generally possess 31 chromosomes. However, some species display dramatic variation in chromosome number. Here we analyse 210 chromosomally complete lepidopteran genomes and show that the chromosomes of extant lepidopterans are derived from 32 ancestral linkage groups, which we term Merian elements. Merian elements have remained largely intact through 250 million years of evolution and diversification. Against this stable background, eight lineages have undergone extensive reorganization either through numerous fissions or a combination of fusion and fission events. Outside these lineages, fusions are rare and fissions are rarer still. Fusions often involve small, repeat-rich Merian elements and the sex-linked element. Our results reveal the constraints on genome architecture in Lepidoptera and provide a deeper understanding of chromosomal rearrangements in eukaryotic genome evolution. Chromosomes are the central units of genome architecture in eukaryotic organisms. They determine processes such as recombination and segregation. While chromosomes are generally stable over evolutionary time, large-scale rearrangements, such as fusions and fissions, can occur. Consequently, chromosomes of extant species can be used to infer the linkage groups present in a common ancestor, termed ancestral linkage groups (ALGs). ALGs have been identified in many taxa including Diptera1, flowering plants2, Nematoda3,4, mammals5, vertebrates6 and Metazoa7. Chromosomal rearrangements have important consequences for genome function8, speciation9 and adaptation10. For example, heterozygous chromosomal fusions can interfere with meiosis, resulting in reproductively isolated populations11,12. The evolutionary forces constraining chromosome number and maintaining ALGs remain unclear. Moreover, how and why certain taxa evade such constraints and experience high rates of karyotypic change are not understood. In monocentric chromosomes, a single region, the centromere, serves as the organizing centre for Mendelian partitioning of homologues during mitosis and meiosis. Discrete centromeres are absent in holocentric chromosomes as centromeric functions are dispersed along the chromosome. Holocentricity has evolved independently 1 , Alexander Mackintosh 1 Article a https://doi.org/10.1038/s41559-024-02329-4 b Lineage with rearrangements c Lineage with complex rearrangements Internal node with rearrangements * Internal node with complex rearrangements Ancient M17 + M20 fusion Noctuidae NOCTUIDEA Erebidae Nolidae Notodontidae Geometridae GEOMETROIDEA Sphingidae Bombycidae Drepanidae Lasiocampidae Crambidae Pyralidae BOMBYCOIDEA DREPANOIDEA PYRALOIDEA Nymphalidae PAPILIONOIDEA Lycaenidae Pieridae Hesperiidae Blastobasidae Depressariidae Pterophoridae Carposinidae * TORTRICOIDEA Tortricidae Ypsolophidae Tineidae Plutellidae Micropterigidae 0.1 0 25 50 75 Haploid chromosome number (n) 0 500 1,000 1,500 2,000 YPONOMEUTOIDEA TINEOIDEA MICROPTERIGOIDEA DITRYSIA Sesiidae Cossidae Zygaenidae GELECHIOIDEA PTEROPHOROIDEA CARPOSINOIDEA SESIOIDEA ZYGAENOIDEA COSSOIDEA APODITRYSIA Papilionidae Genome size (Mb) Fig. 1 | Phylogenetic relationships of 210 lepidopteran species and the distribution of large-scale rearrangement events. a, Phylogeny was inferred using the amino acid sequences of 4,947 orthologues that were present and single copy in 90% of all species sampled under the LG substitution model with gamma-distributed rate variation among sites. The tree was rooted using five representative species of the two main suborders from the sister group, Trichoptera (caddisflies). Excluding the ancient fusion between M17 and M20, which is shared by all Ditrysians (purple asterisk), half of the species have retained intact Merian elements since the last common ancestor of Lepidoptera (black lines). Orange branches indicate lineages with at least one fusion or fission event. Orange circles indicate internal nodes where descendants share a fusion event. We inferred no fission events at internal orange nodes. Red branches indicate lineages with extensively reorganized genomes (Lysandra coridon, Lysandra bellargus, Pieris brassicae, Pieris napi, Pieris rapae, Tinea semifulvella, Melinaea menophilus, Melinaea marsaeus, Aporia crataegi, Brenthis ino, Operophtera brumata, Philereme vetulata, Leptidea sinapis and Apeira syringaria). Red nodes indicate internal nodes where extensively reorganized descendants share fusion or fission events. Scale in substitutions per site is shown. b,c, The distribution of haploid chromosome number (n) (b) and genome size (Mb) (c) across 210 lepidopteran species. Alternating shades distinguish different taxonomic families. Source data for this figure can be found in Supplementary Tables 1 and 6 and in the Zenodo repository122. tends to be one crossover event per chromosome per generation30–32. Thus, loci on a fused chromosome formed from two equally sized progenitors will experience a 50% reduction in per base recom (...truncated)